Ecology

Carvalho, G. R. & Hauser, L. Molecular genetics and the stock concept in fisheries. In Molecular Genetics in Fisheries (eds Carvalho, G. R. & Pitcher, T. J.) 55–79 (Springer Netherlands, 1995). https://doi.org/10.1007/978-94-011-1218-5_3.Chapter 

Google Scholar 
Avise, J. C. Conservation genetics in the marine realm. J. Hered. 89, 377–382 (1998).Article 

Google Scholar 
Waples, R. S. Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species. J. Hered. 89, 438–450 (1998).Article 

Google Scholar 
Pecoraro, C. et al. The population genomics of yellowfin tuna (Thunnus albacares) at global geographic scale challenges current stock delineation. Sci. Rep. 8, 13890 (2018).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Nikolic, N. et al. Connectivity and population structure of albacore tuna across southeast Atlantic and southwest Indian Oceans inferred from multidisciplinary methodology. Sci. Rep. 10, 15657 (2020).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Anderson, G., Lal, M., Hampton, J., Smith, N. & Rico, C. Close kin proximity in yellowfin tuna (Thunnus albacares) as a driver of population genetic structure in the tropical western and central Pacific Ocean. Front. Mar. Sci. 6, 341 (2019).Article 

Google Scholar 
Collette, B. B. & Nauen, C. E. Scombrids of the World: An Annotated and Illustrated Catalogue of Tunas, Mackerels, Bonitos, and Related Species Known to date v.2 (FAO, 1983).
Google Scholar 
Majkowski, J., Arrizabalaga, H. & Carocci, F. C1. Tuna and Tuna-like Species. Review of the state of World Fisheries Resources (FAO, 2005).Mahon, R. Fisheries and research for tunas and tuna-like species in the Western Central Atlantic: implications of the agreement for the implementation of the provisions of the United Nations Convention on the Law of the Sea of the 10 December 1982 relating to the conservation and management of straddling fish stocks and highly migratory fish stocks. (FAO Fisheries Technical Paper, 1996).Doray, M., Stéquert, B. & Taquet, M. Age and growth of blackfin tuna (Thunnus atlanticus ) caught under moored fish aggregating devices, around Martinique Island. Aquat. Living Resour. 17, 13–18 (2004).Article 

Google Scholar 
Arocha, F., Barrios, A. & Marcano, J. Blackfin tuna (Thunnus atlanticus) in the Venezuelan fisheries. Collect. Vol. Sci. Pap ICCAT 68(3), 1253–1260 (2012).
Google Scholar 
Mathieu, H., Pau, C. & Reynal, L. Chapter 2.1.10.7 THON A NAGEOIRES NOIRES. ICCAT ICCAT Manual. International Commission for the Conservation of Atlantic Tuna. 15 (2013).Maghan, W. B. & Rivas, L. R. The blackfin tuna (Thunnus atlanticus) as an underutilized fishery resource in the tropical western Atlantic Ocean. FAO Fish. Rep. 71(2), 163–172 (1971).
Google Scholar 
De Sylva, D. P., Rathjen, W. F. & Higman, J. B. Fisheries development for underutilized Atlantic tunas: Blackfin and little tunny. NOAA Technical Memorandum NMFS-SEFC-191 (1987).Richardson, D. E., Llopiz, J. K., Guigand, C. M. & Cowen, R. K. Larval assemblages of large and medium-sized pelagic species in the Straits of Florida. Prog. Oceanogr. 86, 8–20 (2010).ADS 
Article 

Google Scholar 
Freire, K. M. F., Lessa, R. & Lins-Oliveira, J. E. Fishery and biology of blackfin tuna Thunnus atlanticus off northeastern Brazil. Gulf Caribb. Res. 17, 15–24 (2005).Article 

Google Scholar 
Vieira, K. R., Oliveira, J. E. L. & Barbalho, M. C. Aspects of the dynamic population of blackfin tuna (Thunnus atlanticus-Lesson, 1831) caught in the Northeast Brazil. Collect. Vol. Sci. Pap ICCAT 58(5), 1623–1628 (2005).
Google Scholar 
FJ Mather, I. I. I. Tunas (genus Thunnus) of the western North Atlantic. Part III. Distribution and behavior of Thunnus species. World Sci. Meeting Biol. Tunas Exper. Pap. Vol. 8, 1–23 (1962)Cornic, M. & Rooker, J. R. Influence of oceanographic conditions on the distribution and abundance of blackfin tuna (Thunnus atlanticus) larvae in the Gulf of Mexico. Fish. Res 201, 1–10 (2018).Article 

Google Scholar 
Block, B. A. et al. Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434, 1121–1127 (2005).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Luckhurst, B. E., Trott, T. & Manuel, S. Landings, seasonality, catch per unit effort, and tag-recapture results of yellowfin tuna and blackfin tuna at Bermuda. Am. Fish. Soc. Symp. 25, 225–234 (2001).
Google Scholar 
Singh-Renton, S. & Renton, J. CFRAMP’s large pelagic fish tagging program. Gulf Caribb. Res. Vol 19, (2007).Cermeño, P. et al. Electronic tagging of Atlantic bluefin tuna (Thunnus thynnus, L.) reveals habitat use and behaviors in the Mediterranean Sea. PLoS ONE 10, e0116638 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Begg, G. A., Friedland, K. D. & Pearce, J. B. Stock identification and its role in stock assessment and fisheries management: An overview. Fish. Res 43, 1–8 (1999).Article 

Google Scholar 
Saxton, B. Historical demography and genetic population structure of theBlackfin tuna (Thunnus atlanticus) from the Northwest Atlantic Ocean and the Gulf of Mexico. Texas A&M University (2009).Antoni, L., Luque, P. L., Naghshpour, K., Reynal, L. & Saillant, E. A. Development and characterization of microsatellite markers for blackfin tuna (Thunnus atlanticus) with the use of Illumina paired-end sequencing. Fish. Bull. 112, 322–325 (2014).Article 

Google Scholar 
Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358 (1984).CAS 
PubMed 

Google Scholar 
Goudet, J. FSTAT (Version 1.2): A computer program to calculate F-statistics. J. Hered 86, 485–486 (1995).Article 

Google Scholar 
Rousset, F. Genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).PubMed 
Article 

Google Scholar 
Guo, S. W. & Thompson, E. A. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361–372 (1992).CAS 
PubMed 
MATH 
Article 

Google Scholar 
Van Oosterhout, C., Huthinson, W. F., Wills, D. P. M. & Shipley, P. Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4, 535–538 (2004).Article 
CAS 

Google Scholar 
Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131, 479–491 (1992).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).PubMed 
Article 

Google Scholar 
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodol.) 57, 289–300 (1995).MathSciNet 
MATH 

Google Scholar 
Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Hubisz, M. J., Falush, D., Stephens, M. & Pritchard, J. K. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9, 1322–1332 (2009).PubMed 
PubMed Central 
Article 

Google Scholar 
Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).PubMed 
PubMed Central 
Article 

Google Scholar 
Dupanloup, I., Schneider, S. & Excoffier, L. A simulated annealing approach to define the genetic structure of populations. Mol. Ecol. 11, 2571–2581 (2002).CAS 
PubMed 
Article 

Google Scholar 
Peakall, R. & Smouse, P. E. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537–2539 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Smouse, P. E. & Peakall, R. Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82(Pt 5), 561–573 (1999).PubMed 
Article 

Google Scholar 
Rousset, F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 1219–1228 (1997).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Bezerra, N. P. A. et al. Reproduction of Blackfin tuna Thunnus atlanticus (Perciformes: Scombridae) in Saint Peter and Saint Paul Archipelago, Equatorial Atlantic, Brazil. Rev. Biol. Trop. 61, 1327–1339 (2013).PubMed 
Article 

Google Scholar 
Fitzpatrick, B. M. Power and sample size for nested analysis of molecular variance. Mol. Ecol. 18, 3961–3966 (2009).PubMed 
Article 

Google Scholar 
Ely, B. et al. Consequences of the historical demography on the global population structure of two highly migratory cosmopolitan marine fishes: The yellowfin tuna (Thunnus albacares) and the skipjack tuna (Katsuwonus pelamis). BMC Evol. Biol. 5, 19 (2005).PubMed 
PubMed Central 
Article 

Google Scholar 
Alvarado Bremer, J. R., Viñas, J., Mejuto, J., Ely, B. & Pla, C. Comparative phylogeography of Atlantic bluefin tuna and swordfish: The combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol. Phylogenet. Evol. 36, 169–187 (2005).CAS 
PubMed 
Article 

Google Scholar 
Hedgecock, D., Barber, P. & Edmands, S. Genetic approaches to measuring connectivity. Oceanography 20, 70–79 (2007).Article 

Google Scholar 
Pruett, C. L., Saillant, E. & Gold, J. R. Historical population demography of red snapper (Lutjanus campechanus) from the northern Gulf of Mexico based on analysis of sequences of mitochondrial DNA. Mar. Biol. 147, 593–602 (2005).CAS 
Article 

Google Scholar 
Saillant, E., Bradfield, S. C. & Gold, J. R. Genetic variation and spatial autocorrelation among young-of-the-year red snapper (Lutjanus campechanus) in the northern Gulf of Mexico. ICES J. Mar. Sci 67, 1240–1250 (2010).Article 

Google Scholar 
Robledo-Arnuncio, J. J. & Rousset, F. Isolation by distance in a continuous population under stochastic demographic fluctuations. J. Evol. Biol. 23, 53–71 (2010).CAS 
PubMed 
Article 

Google Scholar 
Rocha, L. A., Craig, M. T. & Bowen, B. W. Phylogeography and the conservation of coral reef fishes. Coral Reefs 26, 501–512 (2007).ADS 
Article 

Google Scholar 
Vasconcellos, A. V., Vianna, P., Paiva, P. C., Schama, R. & Solé-Cava, A. Genetic and morphometric differences between yellowtail snapper (Ocyurus chrysurus, Lutjanidae) populations of the tropical West Atlantic. Genet. Mol. Biol. 31, 308–316 (2008).CAS 
Article 

Google Scholar 
Vieira, K. R., Oliveira, J. E. L. & Barbalho, M. C. Reproductive characteristics of blackfin tuna Thunnus atlanticus (Lesson, 1831), in northeast Brazil. Collect. Vol. Sci. Pap ICCAT 58, 1629–1634 (2005).
Google Scholar 
Nielsen, E. E. et al. Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evol. Biol. 9, 276 (2009).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Lamichhaney, S. et al. Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc. Natl. Acad. Sci. USA 109, 19345–19350 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Latch, E. K., Dharmarajan, G., Glaubitz, J. C. & Rhodes, O. E. Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv. Genet. 7, 295–302 (2006).Article 

Google Scholar 
Brophy, D., Rodríguez-Ezpeleta, N., Fraile, I. & Arrizabalaga, H. Combining genetic markers with stable isotopes in otoliths reveals complexity in the stock structure of Atlantic bluefin tuna (Thunnus thynnus). Sci. Rep. 10, 14675 (2020).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar  More

Spalding, M. D. & Grenfell, A. M. New estimates of global and regional coral reef areas. Coral Reefs 16, 225–230 (1997).Article 

Google Scholar 
Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).Article 

Google Scholar 
Roberts, C. M. et al. Marine Biodiversity Hotspots and Conservation Priorities for Tropical Reefs. Science 295, 1280–1284 (2002).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Johannes, R., Wiebe, W., Crossland, C., Rimmer, D. & Smith, S. Latitudinal limits of coral reef growth. Mar. Ecol. Prog. Ser. 11, 105–111 (1983).ADS 
Article 

Google Scholar 
Kleypas, J. A., Mcmanus, J. W. & Meñez, L. A. B. Environmental Limits to Coral Reef Development: Where Do We Draw the Line? Am. Zool. 39, 146–159 (1999).Article 

Google Scholar 
Yamano, H., Hori, K., Yamauchi, M., Yamagawa, O. & Ohmura, A. Highest-latitude coral reef at Iki Island, Japan. Coral Reefs 20, 9–12 (2001).Article 

Google Scholar 
Guan, Y., Hohn, S. & Merico, A. Suitable Environmental Ranges for Potential Coral Reef Habitats in the Tropical Ocean. PLOS ONE 10, e0128831 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Bellwood, D. R. & Hughes, T. P. Regional-Scale Assembly Rules and Biodiversity of Coral Reefs. Science 292, 1532–1535 (2001).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Connolly, S. R., Bellwood, D. R. & Hughes, T. P. Indo-Pacific Biodiversity of Coral Reefs: Deviations from a Mid-Domain Model. Ecology 84, 2178–2190 (2003).Article 

Google Scholar 
Bellwood, D. R., Hughes, T. P., Connolly, S. R. & Tanner, J. Environmental and geometric constraints on Indo‐Pacific coral reef biodiversity. Ecol. Lett. 8, 643–651 (2005).Article 

Google Scholar 
Kiessling, W., Simpson, C., Beck, B., Mewis, H. & Pandolfi, J. M. Equatorial decline of reef corals during the last Pleistocene interglacial. Proc. Natl Acad. Sci. 109, 21378–21383 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Veron, J. E. N. et al. Delineating the Coral Triangle. Galaxea. J. Coral Reef. Stud. 11, 91–100 (2009).Article 

Google Scholar 
Briggs, J. C. Marine Longitudinal Biodiversity: Causes and Conservation. Divers. Distrib. 13, 544–555 (2007).Article 

Google Scholar 
Renema, W. et al. Hopping Hotspots: Global Shifts in Marine Biodiversity. Science 321, 654–657 (2008).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Kiessling, W. Paleoclimatic significance of Phanerozoic reefs. Geology 29, 751–754 (2001).ADS 
Article 

Google Scholar 
Wallace, C. & Rosen, B. Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: Implications for the evolution of modern diversity patterns of reef corals. Proc. Biol. Sci. 273, 975–982 (2006).PubMed 
PubMed Central 

Google Scholar 
Perrin, C. & Kiessling, W. Latitudinal trends in Cenozoic reef patterns and their relationship to climate. Carbonate Syst. Oligocene–Miocene Clim. Transit. 17–33 (Wiley-Blackwell, 2010).Kiessling, W. Habitat effects and sampling bias on Phanerozoic reef distribution. Facies 51, 24–32 (2005).Article 

Google Scholar 
Kiessling, W. Reef expansion during the Triassic: Spread of photosymbiosis balancing climatic cooling. Palaeogeogr. Palaeoclimatol. Palaeoecol. 290, 11–19 (2010).Article 

Google Scholar 
Ziegler, A. M., Hulver, M. L., Lotts, A. L. & Schmachtenberg, W. F. Uniformitarianism and palaeoclimates: inferences from the distribution of carbonate rocks. In: Fossils and Climate (ed. Brenchley, P. J.), 3–25 (Wiley, Chichester, 1984).Crame, J. A. & Rosen, B. R. Cenozoic palaeogeography and the rise of modern biodiversity patterns. Geol. Soc. Lond. Spec. Publ. 194, 153–168 (2002).ADS 
Article 

Google Scholar 
Leprieur, F. et al. Plate tectonics drive tropical reef biodiversity dynamics. Nat. Commun. 7, 1–8 (2016).Article 
CAS 

Google Scholar 
Zaffos, A., Finnegan, S. & Peters, S. E. Plate tectonic regulation of global marine animal diversity. Proc. Natl Acad. Sci. U. S. A. 114, 5653–5658 (2017).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Roberts, G. G. & Mannion, P. D. Timing and periodicity of Phanerozoic marine biodiversity and environmental change. Sci. Rep. 9, 6116 (2019).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Valentine, J. W. & Moores, E. M. Global Tectonics and the Fossil Record. J. Geol. 80, 167–184 (1972).ADS 
Article 

Google Scholar 
Pellissier, L., Heine, C., Rosauer, D. F. & Albouy, C. Are global hotspots of endemic richness shaped by plate tectonics? Biol. J. Linn. Soc. 123, 247–261 (2017).Article 

Google Scholar 
Chittaro, P. M. Species-area relationships for coral reef fish assemblages of St. Croix, US Virgin Islands. Mar. Ecol. Prog. Ser. 233, 253–261 (2002).ADS 
Article 

Google Scholar 
Tittensor, D. P., Micheli, F., Nyström, M. & Worm, B. Human impacts on the species–area relationship in reef fish assemblages. Ecol. Lett. 10, 760–772 (2007).PubMed 
Article 

Google Scholar 
Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Huntington, B. E. & Lirman, D. Species-area relationships in coral communities: evaluating mechanisms for a commonly observed pattern. Coral Reefs 31, 929–938 (2012).ADS 
Article 

Google Scholar 
Kiessling, W., Simpson, C. & Foote, M. Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 327, 196–198 (2010).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Pandolfi, J. M. et al. Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems. Science 301, 955–958 (2003).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Hoegh-Guldberg, O. Coral reef ecosystems and anthropogenic climate change. Reg. Environ. Change 11, 215–227 (2011).Article 

Google Scholar 
Hughes, T. P. et al. Global warming and recurrent mass bleaching of corals. Nature 543, 373–377 (2017).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Kim, S. W. et al. Refugia under threat: Mass bleaching of coral assemblages in high-latitude eastern Australia. Glob. Change Biol. 25, 3918–3931 (2019).ADS 
Article 

Google Scholar 
Pörtner, H.-O. et al. IPCC special report on the ocean and cryosphere in a changing climate. IPCC Intergov. Panel Clim. Change Geneva Switz. 1, 1–755 (2019).Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264 (2019).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Couce, E., Ridgwell, A. & Hendy, E. J. Future habitat suitability for coral reef ecosystems under global warming and ocean acidification. Glob. Change Biol. 19, 3592–3606 (2013).ADS 
Article 

Google Scholar 
Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W. & Dove, S. Coral Reef Ecosystems under Climate Change and Ocean Acidification. Front. Mar. Sci. 4, 1–20 (2017).O’Neill, B. C. et al. The Scenario Model Intercomparison Project (ScenarioMIP) for CMIP6. Geosci. Model Dev. 9, 3461–3482 (2016).ADS 
Article 

Google Scholar 
Precht, W. F. & Aronson, R. B. Climate flickers and range shifts of reef corals. Front. Ecol. Environ. 2, 307–314 (2004).Article 

Google Scholar 
Greenstein, B. J. & Pandolfi, J. M. Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Glob. Change Biol. 14, 513–528 (2008).ADS 
Article 

Google Scholar 
Pellissier, L. et al. Quaternary coral reef refugia preserved fish diversity. Science 344, 1016–1019 (2014).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Vilhena, D. A. & Smith, A. B. Spatial Bias in the Marine Fossil Record. PLoS ONE 8, 1–7 (2013).Article 
CAS 

Google Scholar 
Close, R. A., Benson, R. B. J., Saupe, E. E., Clapham, M. E. & Butler, R. J. The spatial structure of Phanerozoic marine animal diversity. Science 368, 420–424 (2020).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Jones, L. A., Dean, C. D., Mannion, P. D., Farnsworth, A. & Allison, P. A. Spatial sampling heterogeneity limits the detectability of deep time latitudinal biodiversity gradients. Proc. R. Soc. B Biol. Sci. 288, 20202762 (2021).Article 

Google Scholar 
Jones, L. A. & Eichenseer, K. Uneven spatial sampling distorts reconstructions of Phanerozoic seawater temperature. Geology (2021) https://doi.org/10.1130/G49132.1.Stolarski, J. et al. The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol. Biol. 11, 1–11 (2011).Article 

Google Scholar 
Frankowiak, K. et al. Photosymbiosis and the expansion of shallow-water corals. Sci. Adv. 2, e1601122 (2016).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Phillips, S. J., Anderson, R. P., Dudík, M., Schapire, R. E. & Blair, M. E. Opening the black box: an open-source release of Maxent. Ecography 40, 887–893 (2017).Article 

Google Scholar 
Phillips, S. J., Anderson, R. P. & Schapire, R. E. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259 (2006).Article 

Google Scholar 
Swets, J. A. Measuring the accuracy of diagnostic systems. Science 240, 1285–1293 (1988).ADS 
MathSciNet 
CAS 
PubMed 
MATH 
Article 

Google Scholar 
Boyce, M. S., Vernier, P. R., Nielsen, S. E. & Schmiegelow, F. K. A. Evaluating resource selection functions. Ecol. Model. 157, 281–300 (2002).Article 

Google Scholar 
Hirzel, A. H., LeLay, G., Helfer, V., Randin, C. & Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Model. 199, 142–152 (2006).Article 

Google Scholar 
Elith, J., Kearney, M. & Phillips, S. The art of modelling range-shifting species. Methods Ecol. Evol. 1, 330–342 (2010).Article 

Google Scholar 
Miller, K. G. et al. The Phanerozoic Record of Global Sea-Level Change. Science 310, 1293–1298 (2005).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Hallam, A., Grose, J. A. & Ruffell, A. H. Palaeoclimatic significance of changes in clay mineralogy across the Jurassic-Cretaceous boundary in England and France. Palaeogeogr. Palaeoclimatol. Palaeoecol. 81, 173–187 (1991).Article 

Google Scholar 
Gröcke, D. R., Price, G. D., Ruffell, A. H., Mutterlose, J. & Baraboshkin, E. Isotopic evidence for Late Jurassic–Early Cretaceous climate change. Palaeogeogr. Palaeoclimatol. Palaeoecol. 202, 97–118 (2003).Article 

Google Scholar 
Royer, D. L., Berner, R. A., Montañez, I. P., Tabor, N. J. & Beerling, D. J. CO2 as a primary driver of Phanerozoic climate. GSA Today 14, 1–10 (2004).
Google Scholar 
Grabowski, J. et al. Magnetic susceptibility and spectral gamma logs in the Tithonian–Berriasian pelagic carbonates in the Tatra Mts (Western Carpathians, Poland): Palaeoenvironmental changes at the Jurassic/Cretaceous boundary. Cretac. Res. 43, 1–17 (2013).Article 

Google Scholar 
Vickers, M. L. et al. The duration and magnitude of Cretaceous cool events: Evidence from the northern high latitudes. GSA Bull. 131, 1979–1994 (2019).CAS 
Article 

Google Scholar 
Hay, W. W. & Floegel, S. New thoughts about the Cretaceous climate and oceans. Earth-Sci. Rev. 115, 262–272 (2012).ADS 
CAS 
Article 

Google Scholar 
Tennant, J. P., Mannion, P. D. & Upchurch, P. Sea level regulated tetrapod diversity dynamics through the Jurassic/Cretaceous interval. Nat. Commun. 7, 12737 (2016).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Schouten, S. et al. Onset of long-term cooling of Greenland near the Eocene-Oligocene boundary as revealed by branched tetraether lipids. Geology 36, 147 (2008).ADS 
Article 

Google Scholar 
Zachos, J. C., Dickens, G. R. & Zeebe, R. E. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451, 279–283 (2008).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Crame, J. A. Taxonomic diversity gradients through geological time. Divers. Distrib. 7, 175–189 (2001).
Google Scholar 
Mannion, P. D., Upchurch, P., Benson, R. B. J. & Goswami, A. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol. 29, 42–50 (2014).PubMed 
Article 

Google Scholar 
Fenton, I. S. et al. The impact of Cenozoic cooling on assemblage diversity in planktonic foraminifera. Philos. Trans. R. Soc. B Biol. Sci. 371, 1–12 (2016).Article 
CAS 

Google Scholar 
Saupe, E. E. et al. Climatic shifts drove major contractions in avian latitudinal distributions throughout the Cenozoic. Proc. Natl Acad. Sci. 116, 12895–12900 (2019).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Hall, R. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. J. Asian Earth Sci. 20, 353–431 (2002).ADS 
Article 

Google Scholar 
Hall, R. Southeast Asia’s changing palaeogeography. Blumea 54, 148–161 (2009).Article 

Google Scholar 
Gaboriau, T. et al. Ecological constraints coupled with deep-time habitat dynamics predict the latitudinal diversity gradient in reef fishes. Proc. R. Soc. B Biol. Sci. 286, 20191506 (2019).Article 

Google Scholar 
Saupe, E. E. et al. Extinction intensity during Ordovician and Cenozoic glaciations explained by cooling and palaeogeography. Nat. Geosci. 13, 65–70 (2020).ADS 
Article 
CAS 

Google Scholar 
Lunt, D. J. et al. DeepMIP: model intercomparison of early Eocene climatic optimum (EECO) large-scale climate features and comparison with proxy data. Clim 17, 203–227 (2021).ADS 

Google Scholar 
Freeman, L. A., Kleypas, J. A. & Miller, A. J. Coral Reef Habitat Response to Climate Change Scenarios. PLoS ONE 8, 1–14 (2013).
Google Scholar 
Foster, G. L., Royer, D. L. & Lunt, D. J. Future climate forcing potentially without precedent in the last 420 million years. Nat. Commun. 8, 1–8 (2017).ADS 
Article 
CAS 

Google Scholar 
Farnsworth, A. et al. Past East Asian monsoon evolution controlled by paleogeography, not CO2. Sci. Adv. 5, 1–13 (2019).Article 
CAS 

Google Scholar 
Zhang, L. et al. Consensus Forecasting of Species Distributions: The Effects of Niche Model Performance and Niche Properties. PLoS ONE 10, 1–18 (2015).
Google Scholar 
Harrison, S. P. et al. Evaluation of CMIP5 palaeo-simulations to improve climate projections. Nat. Clim. Change 5, 735–743 (2015).ADS 
Article 

Google Scholar 
Seo, C., Thorne, J. H., Hannah, L. & Thuiller, W. Scale effects in species distribution models: implications for conservation planning under climate change. Biol. Lett. 5, 39–43 (2009).PubMed 
Article 

Google Scholar 
Couce, E., Ridgwell, A. & Hendy, E. J. Environmental controls on the global distribution of shallow-water coral reefs. J. Biogeogr. 39, 1508–1523 (2012).Article 

Google Scholar 
Laborel, J. West African reef corals: an hypothesis on their origin. in Proceedings of the Second International Coral Reef Symposium vol. 1 425–443 (Great Barrier Reef Committee Brisbane, 1974).Spalding, M., Spalding, M. D., Ravilious, C. & Green, E. P. World Atlas of Coral Reefs. (University of California Press, 2001).Block, S. et al. Where to Dig for Fossils: Combining Climate-Envelope, Taphonomy and Discovery Models. PLoS ONE 11, 1–16 (2016).Jones, L. A. et al. Coupling of palaeontological and neontological reef coral data improves forecasts of biodiversity responses under global climatic change. R. Soc. Open Sci. 6, 182111 (2019).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Kusumoto, B. et al. Global distribution of coral diversity: Biodiversity knowledge gradients related to spatial resolution. Ecol. Res. 35, 315–326 (2020).Article 

Google Scholar 
Muir, P. R., Wallace, C. C., Done, T. & Aguirre, J. D. Limited scope for latitudinal extension of reef corals. Science 348, 1135–1138 (2015).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Sillero, N. & Barbosa, A. M. Common mistakes in ecological niche models. Int. J. Geogr. Inf. Sci. 35, 213–226 (2021).Article 

Google Scholar 
Valdes, P. J. et al. The BRIDGE HadCM3 family of climate models:HadCM3@Bristol v1.0. Geosci. Model Dev. 10, 3715–3743 (2017).ADS 
CAS 
Article 

Google Scholar 
Sheppard, C. R. C. Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425, 294–297 (2003).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Saupe, E. E. et al. Macroevolutionary consequences of profound climate change on niche evolution in marine molluscs over the past three million years. Proc. R. Soc. B Biol. Sci. 281, 1–9 (2014).
Google Scholar 
Haywood, A. M. et al. What can Palaeoclimate Modelling do for you? Earth Syst. Environ. 3, 1–18 (2019).Article 

Google Scholar 
Sellwood, B. W. & Valdes, P. J. Mesozoic climates: General circulation models and the rock record. Sediment. Geol. 190, 269–287 (2006).ADS 
Article 

Google Scholar 
Waterson, A. M. et al. Modelling the climatic niche of turtles: a deep-time perspective. Proc. R. Soc. B Biol. Sci. 283, 1–9 (2016).
Google Scholar 
Chiarenza, A. A. et al. Ecological niche modelling does not support climatically-driven dinosaur diversity decline before the Cretaceous/Paleogene mass extinction. Nat. Commun. 10, 1–14 (2019).CAS 
Article 

Google Scholar 
Dunne, E. M., Farnsworth, A., Greene, S. E., Lunt, D. J. & Butler, R. J. Climatic drivers of latitudinal variation in Late Triassic tetrapod diversity. Palaeontology 64, 101–117 (2020).Article 

Google Scholar 
Lyster, S. J., Whittaker, A. C., Allison, P. A., Lunt, D. J. & Farnsworth, A. Predicting sediment discharges and erosion rates in deep time—examples from the late Cretaceous North American continent. Basin Res. 1–27 (2020) https://doi.org/10.1111/bre.12442.Lunt, D. J. et al. Palaeogeographic controls on climate and proxy interpretation. Clim 12, 1181–1198 (2016).ADS 

Google Scholar 
Vasquez, V. L., de Lima, A. A., dos Santos, A. P. & Pinto, M. P. Influence of spatial extent on habitat suitability models for primate species of Atlantic Forest. Ecol. Inform. 61, 101179 (2021).Article 

Google Scholar 
Collins, D. S. et al. Controls on tidal sedimentation and preservation: Insights from numerical tidal modelling in the Late Oligocene–Miocene South China Sea, Southeast Asia. Sedimentology 65, 2468–2505 (2018).Article 

Google Scholar 
Dean, C. D., Collins, D. S., van Cappelle, M., Avdis, A. & Hampson, G. J. Regional-scale paleobathymetry controlled location, but not magnitude, of tidal dynamics in the Late Cretaceous Western Interior Seaway, USA. Geology 47, 1083–1087 (2019).ADS 
CAS 
Article 

Google Scholar 
Markwick, P. J. & Valdes, P. J. Palaeo-digital elevation models for use as boundary conditions in coupled ocean–atmosphere GCM experiments: a Maastrichtian (late Cretaceous) example. Palaeogeogr. Palaeoclimatol. Palaeoecol. 213, 37–63 (2004).Article 

Google Scholar 
Elith, J. et al. Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129–151 (2006).Article 

Google Scholar 
Sillero, N. What does ecological modelling model? A proposed classification of ecological niche models based on their underlying methods. Ecol. Model. 222, 1343–1346 (2011).Article 

Google Scholar 
Guisan, A., Thuiller, W. & Zimmermann, N. E. Habitat suitability and distribution models: with applications in R. (Cambridge University Press, 2017).Kearney, M. R., Wintle, B. A. & Porter, W. P. Correlative and mechanistic models of species distribution provide congruent forecasts under climate change. Conserv. Lett. 3, 203–213 (2010).Article 

Google Scholar 
Owens, H. L. et al. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263, 10–18 (2013).Article 

Google Scholar 
Franklin, J. Mapping Species Distributions: Spatial Inference and Prediction. (Cambridge University Press, 2010). https://doi.org/10.1017/CBO9780511810602.Liu, C., White, M. & Newell, G. Selecting thresholds for the prediction of species occurrence with presence-only data. J. Biogeogr. 40, 778–789 (2013).Article 

Google Scholar 
Liu, C., Newell, G. & White, M. On the selection of thresholds for predicting species occurrence with presence-only data. Ecol. Evol. 6, 337–348 (2016).PubMed 
Article 

Google Scholar 
Kiessling, W. & Krause, M. C. PARED—An online database of Phanerozoic reefs. https://www.paleo-reefs.pal.uni-erlangen.de/ (2021).Jones, L. A., Mannion, P. D., Farnsworth, A., Bragg, F. & Lunt, D. J. Code from ‘Climatic and tectonic drivers shaped the tropical distribution of coral reefs’. Zenodo (2022) https://doi.org/10.5281/zenodo.6458366. More

RESEARCH HIGHLIGHT
14 June 2022

Insects, spiders and other creepy crawlies leave traces of their DNA in dried herbs and other products. More

Frick, W. F. et al. An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682 (2010).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Froschauer, A. & Coleman, J. North American bat death toll exceeds 5.5 million from white-nose syndrome. Biol. Rep. US Fish Wildl. Serv. 2, 1–2 (2012).
Google Scholar 
Blehert, D. S. et al. Bat white-nose syndrome: An emerging fungal pathogen?. Science 323, 227 (2009).CAS 
PubMed 
Article 

Google Scholar 
Meteyer, C. U. et al. Histopathologic criteria to confirm white-nose syndrome in bats. J. Vet. Diagn. Invest. 21, 411–414 (2009).PubMed 
Article 

Google Scholar 
O’Donoghue, A. J. et al. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. Proc. Natl. Acad. Sci. USA. 112, 7478–7483 (2015).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Cryan, P. M., Meteyer, C. U., Boyles, J. G. & Blehert, D. S. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. BMC Biol. 8, 135 (2010).PubMed 
PubMed Central 
Article 

Google Scholar 
Warnecke, L. et al. Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality. Biol. Lett. 9, 20130177 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Verant, M. L., Boyles, J. G., Waldrep, W., Wibbelt, G. & Blehert, D. S. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE 7, e46280 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Field, K. A. et al. The white-nose syndrome transcriptome: Activation of anti-fungal host responses in wing tissue of hibernating little brown Myotis. PLoS Pathog. 11, e1005168 (2015).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Boyles, J. G. & Willis, C. K. R. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome?. Front. Ecol. Environ. 8, 92–98 (2010).Article 

Google Scholar 
Storm, J. J. & Boyles, J. G. Body temperature and body mass of hibernating little brown bats Myotis lucifugus in hibernacula affected by white-nose syndrome. Acta Theriol. 56, 123–127 (2011).Article 

Google Scholar 
Lorch, J. M. et al. First detection of bat white-nose syndrome in western North America. MSphere 1, 4 (2016).Article 
CAS 

Google Scholar 
White-Nose Syndrome Response Team. Where is WNS Now? White-Nose Syndrome https://www.whitenosesyndrome.org/spreadmap (2021).Turner, G. G., Reeder, D. & Coleman, J. T. H. A five-year assessment of mortality and geographic spread of white-nose syndrome in north American bats, with a look at the future: update of white-nose syndrome in bats. Bat Res. News 52, 13 (2011).
Google Scholar 
Dzal, Y., McGuire, L. P., Veselka, N. & Fenton, M. B. Going, going, gone: The impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus). Biol. Lett. 7, 392–394 (2011).PubMed 
Article 

Google Scholar 
Ingersoll, T. E., Sewall, B. J. & Amelon, S. K. Improved analysis of long-term monitoring data demonstrates marked regional declines of bat populations in the eastern United States. PLoS ONE 8, e65907 (2013).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Vanderwolf, K. J. & McAlpine, D. F. Hibernacula microclimate and declines in overwintering bats during an outbreak of white-nose syndrome near the northern range limit of infection in North America. Ecol. Evol. 11, 2273–2288 (2021).PubMed 
PubMed Central 
Article 

Google Scholar 
Boyles, J. G., Cryan, P. M., McCracken, G. F. & Kunz, T. H. Economic importance of bats in agriculture. Science 332, 41–42 (2011).ADS 
PubMed 
Article 

Google Scholar 
Kunz, T. H., de Torrez, E. B., Bauer, D., Lobova, T. & Fleming, T. H. Ecosystem services provided by bats. Ann. N. Y. Acad. Sci. 1223, 1–38 (2011).ADS 
PubMed 
Article 

Google Scholar 
Puig‐Montserrat, X. & Flaquer, C. Bats actively prey on mosquitoes and other deleterious insects in rice paddies: Potential impact on human health and agriculture. Pest Manag. Sci. (2020).Micalizzi, E. W. & Smith, M. L. Volatile organic compounds kill the white-nose syndrome fungus, Pseudogymnoascus destructans, in hibernaculum sediment. Can. J. Microbiol. 66, 593–599 (2020).CAS 
PubMed 
Article 

Google Scholar 
Padhi, S., Dias, I., Korn, V. & Bennett, J. Pseudogymnoascus destructans: Causative agent of white-nose syndrome in bats is inhibited by safe volatile organic compounds. Journal of Fungi 4, 48 (2018).PubMed Central 
Article 
CAS 

Google Scholar 
Chaturvedi, S. et al. Antifungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of geomycosis (WNS) in bats. PLoS ONE 6, e17032 (2011).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Cornelison, C. T. et al. A preliminary report on the contact-independent antagonism of Pseudogymnoascus destructans by Rhodococcus rhodochrous strain DAP96253. BMC Microbiol. 14, 246 (2014).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Boire, N. et al. Potent inhibition of Pseudogymnoascus destructans, the causative agent of white-nose syndrome in bats, by cold-pressed, terpeneless, Valencia orange oil. PLoS ONE 11, 1–10 (2016).Article 
CAS 

Google Scholar 
Padhi, S., Dias, I. & Bennett, J. W. Two volatile-phase alcohols inhibit growth of Pseudogymnoascus destructans, causative agent of white-nose syndrome in bats. Mycology 8, 11–16 (2017).CAS 
Article 

Google Scholar 
Raudabaugh, D. B. & Miller, A. N. Effect of Trans, trans-farnesol on Pseudogymnoascus destructans and several closely related species. Mycopathologia 180, 325–332 (2015).CAS 
PubMed 
Article 

Google Scholar 
Kulhanek. The Application of Chitosan on an Experimental Infection of Pseudogymnoascus Destructans Increases Survival in Little Brown Bats. (Western Michigan University, 2016).Ghosh, S. et al. Evidence for Anti-Pseudogymnoascus destructans (Pd) activity of propolis. Antibiotics 7, 2 (2017).PubMed Central 
Article 
CAS 

Google Scholar 
Bernard, R. F. & Grant, E. H. C. Identifying common decision problem elements for the management of emerging fungal diseases of wildlife. Soc. Nat. Resour. (2019).Haas, D. & Défago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3, 307–319 (2005).CAS 
PubMed 
Article 

Google Scholar 
Becker, M. H. & Harris, R. N. Cutaneous bacteria of the redback salamander prevent morbidity associated with a lethal disease. PLoS ONE 5, e10957 (2010).ADS 
PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Gerritsen, J., Smidt, H., Rijkers, G. T. & de Vos, W. M. Intestinal microbiota in human health and disease: The impact of probiotics. Genes Nutr. 6, 209–240 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
Bletz, M. C. et al. Mitigating amphibian chytridiomycosis with bioaugmentation: Characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16, 807–820 (2013).PubMed 
Article 

Google Scholar 
Becker, M. H. et al. Composition of symbiotic bacteria predicts survival in Panamanian golden frogs infected with a lethal fungus. Proc. Biol. Sci. 282, 2881 (2015).
Google Scholar 
Hamm, P. S. et al. Western bats as a reservoir of novel Streptomyces species with antifungal activity. Appl. Environ. Microbiol. 83, 1–10 (2017).Article 

Google Scholar 
Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE https://doi.org/10.1371/journal.pone.0121329 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Cheng, T. L. et al. Efficacy of a probiotic bacterium to treat bats affected by the disease white-nose syndrome. J. Appl. Ecol. 54, 701–708 (2017).Article 

Google Scholar 
Berg, G. & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1–13 (2009).CAS 
PubMed 
Article 

Google Scholar 
Teplitski, M. & Ritchie, K. How feasible is the biological control of coral diseases?. Trends Ecol. Evol. 24, 378–385 (2009).PubMed 
Article 

Google Scholar 
Clay, K. EDITORIAL: Defensive symbiosis: A microbial perspective. Funct. Ecol. 28, 293–298 (2014).Article 

Google Scholar 
Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl. Acad. Sci. USA. 111, E5049–E5058 (2014).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Lemieux-Labonté, V., Simard, A., Willis, C. K. R. & Lapointe, F.-J. Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5, 115 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Walke, J. B. et al. Most of the dominant members of amphibian skin bacterial communities can be readily cultured. Appl. Environ. Microbiol. 81, 6589–6600 (2015).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Avena, C. V. et al. Deconstructing the bat skin microbiome: Influences of the host and the environment. Front. Microbiol. 7, 1753 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
Loudon, A. H. et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME J. 8, 830–840 (2014).CAS 
PubMed 
Article 

Google Scholar 
Walke, J. B. et al. Amphibian skin may select for rare environmental microbes. ISME J. 8, 2207–2217 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Loudon, A. H. et al. Vertebrate hosts as islands: Dynamics of selection, immigration, loss, persistence, and potential function of bacteria on salamander skin. Front. Microbiol. 7, 333 (2016).PubMed 
PubMed Central 
Article 

Google Scholar 
Winter, A. S. et al. Skin and fur bacterial diversity and community structure on American southwestern bats: Effects of habitat, geography and bat traits. PeerJ 5, e3944 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Perofsky, A. C., Lewis, R. J., Abondano, L. A., Di Fiore, A. & Meyers, L. A. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. Proc. Biol. Sci. 284, 2274 (2017).
Google Scholar 
Raulo, A. et al. Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality. J. Anim. Ecol. 87, 388–399 (2018).PubMed 
Article 

Google Scholar 
Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. Elife 4, 5224 (2015).
Google Scholar 
Kolodny, O. et al. Coordinated change at the colony level in fruit bat fur microbiomes through time. Nat. Ecol. Evol. 3, 116–124 (2019).PubMed 
Article 

Google Scholar 
Vuong, H. E., Yano, J. M., Fung, T. C. & Hsiao, E. Y. The microbiome and host behavior. Annu. Rev. Neurosci. 40, 21–49 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Lausen, C. L., Nagorsen, D. N., Brigham, R. M. & Hobbs, J. Bats of British Columbia 2nd edn. (Royal BC Museum, 2022).
Google Scholar 
Spring Cleaning: Why Wash a Bridge? https://www.tranbc.ca/2011/06/22/spring-cleaning-why-wash-a-bridge/ (2012).Maron, P.-A. et al. High microbial diversity promotes soil ecosystem functioning. Appl. Environ. Microbiol. 84, 9 (2018).Article 

Google Scholar 
Wagg, C., Bender, S. F., Widmer, F. & van der Heijden, M. G. A. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. USA. 111, 5266–5270 (2014).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Green, S. R. & Gray, P. P. A differential procedure for bacteriological studies useful in the fermentation industry. Arch. Biochem. Biophys. 32, 59–69 (1951).CAS 
PubMed 
Article 

Google Scholar 
Basu, S. et al. Evolution of bacterial and fungal growth media. Bioinformation 11, 182–184 (2015).PubMed 
PubMed Central 
Article 

Google Scholar 
Medina, D. et al. Culture media and individual hosts affect the recovery of culturable bacterial diversity from amphibian skin. Front. Microbiol. 8, 1574 (2017).PubMed 
PubMed Central 
Article 

Google Scholar 
Piovia-Scott, J. et al. Greater species richness of bacterial skin symbionts better suppresses the amphibian fungal pathogen Batrachochytrium dendrobatidis. Microb. Ecol. 74, 217–226 (2017).PubMed 
Article 

Google Scholar 
Moeller, A. H. et al. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc. Natl. Acad. Sci. USA. 114, 13768–13773 (2017).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Ingala, M. R. et al. Comparing microbiome sampling methods in a wild mammal: Fecal and intestinal samples record different signals of host ecology, evolution. Front. Microbiol. 9, 1–10 (2018).Article 

Google Scholar 
Lewis, S. E. Night roosting ecology of pallid bats (Antrozous pallidus) in oregon. Am. Midl. Nat. 132, 219–226 (1994).Article 

Google Scholar 
Hershey, O. S. & Barton, H. A. The microbial diversity of caves. Cave Ecol. 1, 69–90. https://doi.org/10.1007/978-3-319-98852-8_5 (2018).Article 

Google Scholar 
British Columbia Government Mineral Inventory. https://www2.gov.bc.ca/gov/content/industry/mineral-exploration-mining/british-columbia-geological-survey/mineralinventory (2018).Weller, T. J. et al. A review of bat hibernacula across the western United States: Implications for white-nose syndrome surveillance and management. PLoS ONE 13, e0205647 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Nagorsen, D. W., Brigham, R. M., Royal British Columbia Museum. Bats of British Columbia (UBC Press, 1993).
Google Scholar 
Fenton, M. B., Merriam, H. G. & Holroyd, G. L. Bats of Kootenay, Glacier, and Mount Revelstoke national parks in Canada: Identification by echolocation calls, distribution, and biology. Can. J. Zool. 61, 2503–2508 (1983).Article 

Google Scholar 
Bernard, R. F., Foster, J. T., Willcox, E. V., Parise, K. L. & McCracken, G. F. Molecular detection of the causative agent of white-nose syndrome on rafinesque’s big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the Southeastern USA. J. Wildl. Dis. 51, 519–522 (2015).PubMed 
Article 

Google Scholar 
Lutz, H. L. et al. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. MSystems 4, 1–10 (2019).
Google Scholar 
Gaona, O., Gómez-Acata, E. S., Cerqueda-García, D., Neri-Barrios, C. X. & Falcón, L. I. Fecal microbiota of different reproductive stages of the central population of the lesser-long nosed bat, Leptonycteris yerbabuenae. PLoS ONE 14, e0219982 (2019).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Voigt, C. C., Caspers, B. & Speck, S. Bats, bacteria, and bat smell: Sex-specific diversity of microbes in a sexually selected scent organ. J. Mammal. 86, 745–749 (2005).Article 

Google Scholar 
Gharout-Sait, A. et al. Occurrence of carbapenemase-producing Klebsiella pneumoniae in bat guano. Microb. Drug Resist. 25, 1057–1062 (2019).CAS 
PubMed 
Article 

Google Scholar 
Sánchez, C. et al. Contribution of citrate metabolism to the growth of Lactococcus lactis CRL264 at low pH. Appl. Environ. Microbiol. 74, 1136–1144 (2008).ADS 
PubMed 
Article 
CAS 

Google Scholar 
Charyulu, E. M. & Gnanamani, A. Condition stabilization for Pseudomonas aeruginosa MTCC 5210 to yield high titers of extra cellular antimicrobial secondary metabolite using response surface methodology. Curr. Res. Bacteriol. 4, 197–213 (2010).Article 

Google Scholar 
Shen, Y. et al. Psychrobacillus lasiicapitis sp. nov., isolated from the head of an ant (Lasius fuliginosus). Int. J. Syst. Evol. Microbiol. 67, 4462–4467 (2017).CAS 
PubMed 
Article 

Google Scholar 
Rodríguez, M., Reina, J. C., Béjar, V. & Llamas, I. Psychrobacillus vulpis sp. nov., a new species isolated from faeces of a red fox in Spain. Int. J. Syst. Evol. Microbiol. 70, 882–888 (2020).PubMed 
Article 
CAS 

Google Scholar 
Pham, V. H. T., Jeong, S.-W. & Kim, J. Psychrobacillus soli sp. nov., capable of degrading oil, isolated from oil-contaminated soil. Int. J. Syst. Evol. Microbiol. 65, 3046–3052 (2015).CAS 
PubMed 
Article 

Google Scholar 
Kontro, M., Lignell, U., Hirvonen, M.-R. & Nevalainen, A. pH effects on 10 Streptomyces spp. growth and sporulation depend on nutrients. Lett. Appl. Microbiol. 41, 32–38 (2005).CAS 
PubMed 
Article 

Google Scholar 
Wodzinski, R. S., Umholtz, T. E., Rundle, J. R. & Beer, S. V. Mechanisms of inhibition of Erwinia amylovora by Erw. herbicola in vitro and in vivo. J. Appl. Bacteriol. 76, 22–29 (1994).Article 

Google Scholar 
Kuncharoen, N. et al. Achromobacter aloeverae sp. nov., isolated from the root of Aloe vera (L.) Burm. f. Int. J. Syst. Evol. Microbiol. 67, 37–41 (2017).CAS 
PubMed 
Article 

Google Scholar 
Aizawa, T. et al. Curtobacterium ammoniigenes sp. nov., an ammonia-producing bacterium isolated from plants inhabiting acidic swamps in actual acid sulfate soil areas of Vietnam. Int. J. Syst. Evol. Microbiol. 57, 1447–1452 (2007).CAS 
PubMed 
Article 

Google Scholar 
Kaira, G. S., Dhakar, K. & Pandey, A. A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range. AMB Express 5, 92 (2015).PubMed 
Article 

Google Scholar 
Moon, J. & Kim, J. Isolation of Paenibacillus pinesoli sp. Nov. from forest soil in Gyeonggi-Do, Korea. J. Microbiol. 52, 273–277 (2014).CAS 
PubMed 
Article 

Google Scholar 
Heyrman, J. et al. Bacillus novalis sp. nov., Bacillus vireti sp. nov., Bacillus soli sp. nov., Bacillus bataviensis sp. nov. and Bacillus drentensis sp. nov., from the Drentse A grasslands. Int. J. Syst. Evol. Microbiol. 54, 47–57 (2004).CAS 
PubMed 
Article 

Google Scholar 
Hughes, K. L. & Sulaiman, I. The ecology of Rhodococcus equi and physicochemical influences on growth. Vet. Microbiol. 14, 241–250 (1987).CAS 
PubMed 
Article 

Google Scholar 
Schrempf, H. Recognition and degradation of chitin by streptomycetes. Antonie Van Leeuwenhoek 79, 285–289 (2001).CAS 
PubMed 
Article 

Google Scholar 
Seco, E. M., Cuesta, T., Fotso, S., Laatsch, H. & Malpartida, F. Two polyene amides produced by genetically modified Streptomyces diastaticus var. 108. Chem. Biol. 12, 535–543 (2005).CAS 
PubMed 
Article 

Google Scholar 
Kembel, S. W., Wu, M., Eisen, J. A. & Green, J. L. Incorporating 16S gene copy number information improves estimates of microbial diversity and abundance. PLoS Comput. Biol. 8, e1002743 (2012).ADS 
CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
León, M. et al. Antifungal activity of selected indigenous pseudomonas and bacillus from the soybean rhizosphere. Int. J. Microbiol. 2009, 572049 (2009).PubMed 
PubMed Central 
Article 

Google Scholar 
Van Hai, N. & Fotedar, R. Comparison of the effects of the prebiotics (Bio-Mos® and β-1, 3-D-glucan) and the customised probiotics (Pseudomonas synxantha and P. aeruginosa) on the culture of juvenile western king prawns (Penaeus latisulcatus Kishinouye, 1896). Aquaculture 289, 310–316 (2009).Article 
CAS 

Google Scholar 
Lauer, A., Simon, M. A., Banning, J. L., Lam, B. A. & Harris, R. N. Diversity of cutaneous bacteria with antifungal activity isolated from female four-toed salamanders. ISME J. 2, 145–157 (2008).CAS 
PubMed 
Article 

Google Scholar 
Ligon, J. M. et al. Natural products with antifungal activity fromPseudomonas biocontrol bacteria. Pest Manag. Sci. 56, 688–695 (2000).CAS 
Article 

Google Scholar 
Scholz-Schroeder, B. K., Hutchison, M. L., Grgurina, I. & Gross, D. C. The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Mol. Plant Microb. Interact. 14, 336–348 (2001).CAS 
Article 

Google Scholar 
Souza, J. T. & Raaijmakers, J. M. Polymorphisms within the prnD and pltC genes from pyrrolnitrin and pyoluteorin-producing Pseudomonas and Burkholderia spp. FEMS Microbiol. Ecol. 43, 21–34 (2003).PubMed 
Article 

Google Scholar 
Mavrodi, D. V. et al. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J. Bacteriol. 183, 6454–6465 (2001).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Diby, P. et al. Mycolytic enzymes produced by Pseudomonas fluorescens and Trichoderma spp. against Phytophthora capsici, the foot rot pathogen of black pepper (Piper nigrum L.). Ann. Microbiol. 55, 129–133 (2005).CAS 

Google Scholar 
Vengust, M., Knapic, T. & Weese, J. S. The fecal bacterial microbiota of bats; Slovenia. PLoS ONE 13, e0196728 (2018).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Banskar, S., Mourya, D. T. & Shouche, Y. S. Bacterial diversity indicates dietary overlap among bats of different feeding habits. Microbiol. Res. 182, 99–108 (2016).PubMed 
Article 

Google Scholar 
Wolkers-Rooijackers, J. C. M., Rebmann, K., Bosch, T. & Hazeleger, W. C. Fecal Bacterial Communities in Insectivorous Bats from the Netherlands and Their Role as a Possible Vector for Foodborne Diseases. Acta Chiropterol. 20, 475 (2019).Article 

Google Scholar 
Weller, T. J., Scott, S. A., Rodhouse, T. J., Ormsbee, P. C. & Zinck, J. M. Field identification of the cryptic vespertilionid bats, Myotis lucifugus and M. yumanensis. Acta Chiropt. 9, 133–147 (2007).Article 

Google Scholar 
Khankhet, J. et al. Clonal expansion of the Pseudogymnoascus destructans genotype in North America is accompanied by significant variation in phenotypic expression. PLoS ONE 9, e104625 (2014).Article 
CAS 

Google Scholar 
McArthur, R. L., Ghosh, S. & Cheeptham, N. Improvement of protocols for the screening of biological control agents against white-nose syndrome. JEMI 2, 1–7 (2017).
Google Scholar 
Rajkumar, S. S. et al. Clonal genotype of Geomyces destructans among bats with white nose syndrome, New York, USA. Emerg. Infect. Dis. 17, 1273–1276 (2011).PubMed 
PubMed Central 
Article 

Google Scholar 
Ren, P. et al. Clonal spread of Geomyces destructans among bats, Midwestern and Southern United States. Emerg. Infect. Dis. 18, 883–885 (2012).PubMed 
PubMed Central 
Article 

Google Scholar 
Wilson, K. Genomc DNA extraction using the modified CTAB method. Curr. Protoc. Mol. Biol. 1, 1–2 (1997).
Google Scholar 
Edwards, U., Rogall, T., Blöcker, H., Emde, M. & Böttger, E. C. Isolation and direct complete nucleotide determination of entire genes: Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res. 17, 7843–7853 (1989).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Stackebrandt, E. & Liesack, W. Handbook of New Bacterial Systematics (Springer, 1993).
Google Scholar 
O’Leary, N. A. et al. Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 44, D733–D745 (2016).PubMed 
Article 
CAS 

Google Scholar 
Camacho, C. et al. BLAST+: Architecture and applications. BMC Bioinformatics 10, 421 (2009).PubMed 
PubMed Central 
Article 
CAS 

Google Scholar 
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Stamatakis, A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2015).Venables, W. N. & Ripley, B. D. Modern applied statistics with S. Stat. Comput. https://doi.org/10.1007/978-0-387-21706-2 (2002).Article 
MATH 

Google Scholar 
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

Google Scholar 
Lenth, R. & Lenth, M. R. Package ‘lsmeans’. Am. Stat. 34, 216–221 (2018).
Google Scholar 
Kassambara, A. ggpubr:‘ggplot2’ based publication ready plots. R package version 0.1. 7 (2018). More

Theodor, J. M., Erfort, J. & Métais, G. The earliest artiodactyls: Diacodexeidae, Dichobunidae, Homacodontidae, Leptochoeridae and Raoellidae. in Evolution of Artiodactyls (eds. Prothero, D.R. & Foss, S. E.). 32–58. (Johns Hopkins University, 2007).Badiola, A. et al. The role of new Iberian finds in understanding European Eocene mammalian paleobiogeography. Geol. Acta. 7(1–2), 243–258 (2009).
Google Scholar 
Boivin, M. et al. New material of Diacodexis (Mammalia, Artiodactyla) from the early Eocene of Southern Europe. Geobios 51(4), 285–306 (2018).Article 

Google Scholar 
Ellenberger, P. Sur les empreintes de pas des gros mammiféres de l’Eocene supérieur de Garrigues-Ste-Eulalie (Gard). Palaeovertebr. Mém. Jubil. R. Lavocat. 13, 37–78 (1980).
Google Scholar 
Santamaría, R. L. G. & Casanovas-Cladellas, M. L. Nuevos yacimientos con icnitas de mamíferos del Oligoceno de los alrededores de Agramunt (Lleida, España). Paleont. Evol. 23, 141–152 (1990).
Google Scholar 
Sarjeant, W. A. S. & Langston, W. Jr. Vertebrate footprints and invertebrate traces from the Chadronian (Late Eocene) of Trans-Pecos. Texas. Mem. Mus. Bull. 36, 1–86 (1994).
Google Scholar 
Costeur, L., Balme, C. & Legal, S. Early Oligocene mammal tracks from southeastern France. Hist. Biol. 16(4), 257–267. https://doi.org/10.1080/10420940902953197 (2009).Article 

Google Scholar 
Wroblewski, A.F.-J. & Gulas-Wroblewski, B. E. Earliest evidence of marine habitat use by mammals. Sci. Rep. 11, 8846. https://doi.org/10.1038/s41598-021-88412-3 (2021).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Fornós, J. J. & Pons-Moya, J. Icnitas de Myotragus balearicus del yacimiento de Ses Piquetes (Santanyi, Mallorca). Bol. Soc. Hist. Nat. Balears 26, 135–144 (1982).
Google Scholar 
Flor, G. Estructuras de deformación por pisadas de cérvidos en la duna cementada de Gorliz (Vizcaya, N de España). Rev. Soc. Geol. Esp. 2(1–2), 23–29 (1989).
Google Scholar 
Fornós, J. J., Bromley, R. G., Clemmensen, L. B. & Rodríguez-Perea, A. Tracks and trackways of Myotragus balearicus Bate (Artiodactyla, Caprinae) in Pleistocene aeolianites from Mallorca (Balearic Islands, Western Mediterranean). Palaeogr. Palaeocl. Palaeoecol. 180, 277–313 (2002).ADS 
Article 

Google Scholar 
Neto de Carvalho, C. Vertebrate tracksites from the Mid-Late Pleistocene eolianites of Portugal: The first record of elephant tracks in Europe. Geol. Q. 53(4), 407–414 (2009).
Google Scholar 
Neto de Carvalho, C., Saltão, S., Ramos, J. C. & Cachão, M. Pegadas de Cervus elaphus nos eolianitos plistocénicos da ilha do Pessegueiro (SW Alentejano, Portugal). Ciênc. Terra 5, 36–40 (2003).
Google Scholar 
Neto de Carvalho, C., Figueiredo, S. & Belo, J. Vertebrate tracks and trackways from the Pleistocene eolianites of SW Portugal. Commun. Geol. 103(1), 101–116 (2016).CAS 

Google Scholar 
Neto de Carvalho, C. et al. Paleoecological implications of large-sized wild boar tracks recorded during the Last Interglacial (MIS 5) at Huelva (SW Spain). Palaios https://doi.org/10.2110/palo.2020.058 (2020).Article 

Google Scholar 
Neto de Carvalho, C. et al. First vertebrate tracks and palaeoenvironment in a MIS-5 context in the Doñana National Park (Huelva, SW Spain). Quat. Sci. Rev. https://doi.org/10.1016/j.quascirev.2020.106508 (2020).Article 

Google Scholar 
Cardoso, J. L. Les grands mammifères du Pléistocène supérieur du Portugal. Essai de synthése. Geobios 29(2), 235–250 (1996).Article 

Google Scholar 
Sala, M. T. N., Pantoja, A., Arsuaga, J. L. & Algaba, M. Presencia de bisonte (Bison priscus Bojanus, 1827) y uro (Bos primigenius Bojanus, 1827) en las cuevas del Búho y de la Zarzamora (Segovia, España). Munibe 61, 43–55 (2010).
Google Scholar 
Figueiredo, S. D. & Sousa, M. F. O registo de bovídeos plistocénicos em Portugal. in Livro de Resumos das IV Jornadas de Arqueologia do Vale do Tejo. Vol. 10. (Centro Português de Geo-História e Pré-História, 2017).Barr, K. & Bell, M. Neolithic and Bronze age ungulate footprint-tracks of the Severn Estuary: Species, age, identification and the interpretation of husbandry practices. Environ. Archaeol. 22(1), 1–15 (2017).Article 

Google Scholar 
Bell, M. Making One’s Way in the World (Oxbow Books, 2020).Book 

Google Scholar 
Díaz-Martínez, I. et al. Multi-aged social behavior based on artiodactyl tracks in an early Miocene palustrine wetland (Ebro Basin, Spain). Sci. Rep. 10, 1099. https://doi.org/10.1038/s41598-020-57438-4 (2020).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Quintana, J. Descripción de un rastro de Myotragus e icnitas de Hypnomys del yacimiento cuaternario de Ses Penyes d’es Perico (Ciutadella de Menorca, Balears). Paleont. Evol. 26–27, 271–279 (1993).
Google Scholar 
Muñiz, F. et al. Following the last Neanderthals: Mammal tracks in Late Pleistocene coastal dunes of Gibraltar (S Iberian Peninsula). Quat. Sci. Rev. 217, 297–309 (2019).ADS 
Article 

Google Scholar 
Altuna, J. Fauna de mamíferos de los yacimientos prehistóricos de Guipúzcoa. Con catálogo de los mamíferos cuaternarios del Cantábrico y del Pirineo occidental. Munibe 24, 1–464 (1972).
Google Scholar 
López González, F., Vila Taboada, M. & Grandal d’Anglade. Sobre los grandes bóvidos pleistocenos (Bovidae, Mammalia) en el NO de la Península Ibérica. Cad. Lab. Xeol. Laxe 24, 57–71 (1999).Sommer, R. S., Kalbe, J., Ekström, J., Benecke, N. & Liljengren, R. Range dynamics of the reindeer in Europe during the last 25,000 years. J. Biogeogr. 41, 298–306. https://doi.org/10.1111/jbi.12193 (2014).Article 

Google Scholar 
Whittle, A., Antoine, S., Gardiner, N., Milles, A. & Webster, A. Two Later Bronze Age occupations and an Iron Age channel on the Gwent foreshore. Bull. Board Celt. Stud. 36, 200–223 (1989).
Google Scholar 
Aldhouse-Green, S. et al. Prehistoric human footprints from the Severn Estuary at Uskmouth and Magor Pill, Gwent, Wales. Archae. Cambr. 141, 4–55 (1992).
Google Scholar 
Allen, J. R. L. Subfossil mammalian tracks (Flandrian) in the Severn Estuary, S.W. Britain: Mechanics of formation, preservation and distribution. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 352(1352), 481–518 (1997).ADS 
PubMed Central 
Article 

Google Scholar 
Bell, M. Prehistoric coastal communities: the Mesolithic in western Britain. in CBA Research Report. Vol. 149. (Council for British Archaeology, 2007).Bell, M. The Bronze Age in the Severn estuary. in Research Report. Vol. 172. (Council for British Archaeology, 2013).Scales, R. Footprint tracks of people and animals. in Prehistoric Coastal Communities: The Mesolithic in Western Britain (ed. Bell, M.). Vol. 149. 139–147. CBA Research Report 149. (Council of British Archaeology, 2007).Roberts, G. Ephemeral, subfossil mammalian, avian and hominid footprints within Flandrian sediment exposures at Formby Point, Sefton Coast, North West England. Ichnos 16, 33–48 (2009).Article 

Google Scholar 
Waddington, C. Low Hauxley, Northumberland: A review of archaeological interventions and site condition. Archael. Res. Serv. 2010/25 (2010).Eadie, G. & Waddington, C. Rescue recording of an eroding inter-tidal peat bed at Lower Hauxley, Northumberland (6109). Archael. Res. Serv. 2013/17 (2013).Burns, A. The prehistoric footprints at Formby. in Sefton Coast Landscape Partnership Scheme (2014).Pandolfi, L., Petronio, C. & Salari, L. Bos primigenius Bojanus, 1827 from the Early Late Pleistocene deposit of Avetrana (southern Italy) and the variation in size of the species in southern Europe: Preliminary report. J. Geol. Res. https://doi.org/10.1155/2011/245408 (2011).Article 

Google Scholar 
Currant, A. P. A review of the Quaternary mammals of Gibraltar. in Neanderthals on the Edge: 150th Anniversary Conference of the Forbes’ Quarry Discovery, Gibraltar (eds. Stringer, C. B., Barton, R. N. E. & Finlayson, J.C.). 201–206. (Oxbow, 2000).Penela, A. J. M. Los grandes mamíferos del yacimiento acheulense de la Solana del Zamborino, Fonelas (Granada, España). Antr. Paleoecol. Hum. 5, 29–187 (1988).
Google Scholar 
Bataille, G. Prehistoric Painting. Lascaux or the Birth of Art (MacMillan, 1980).
Google Scholar 
Zazo, C. et al. Palaeoenvironmental evolution of the Barbate-Trafalgar coast (Cadiz) during the last ~140 ka: Climate, sea-level interactions and tectonics. Geomorphology 100, 212–222 (2008).ADS 
Article 

Google Scholar 
Zazo, C. et al. Landscape evolution and geodynamic controls in the Gulf of Cadiz (Huelva coast, SW Spain) during the Late Quaternary. Geomorphology 68, 269–290. https://doi.org/10.1016/j.geomorph.2004.11.022 (2005).ADS 
Article 

Google Scholar 
García de Domingo, A., González Lastra, J., Hernaiz Huerta, P. P., Zazo Cardeña, C. & Goy Goy, J. L. Mapa Geológico de la Hoja No. 1073 (Vejer de la Frontera). Mapa Geológico de España a Escala 1:50.000. Segunda Serie (MAGNA). http://info.igme.es/cartografiadigital/geologica/Magna50Hoja.aspx?Id=1073&language=es (©Instituto Geológico y Minero de España (IGME), 1990).Demathieu, G., Ginsburg, L., Guérin, C. & Truc, G. Étude paléontologique, ichnologique et paléoécologique du gisêment oligocène de Saignon (bassin d’Apt, Vaucluse). Bull. Mus. Natl. Hist. Nat. 6(2), 153–183 (1984).
Google Scholar 
Bang, P. & Dahlstrøm, P. Animal Tracks and Signs (Oxford University Press, 2001).
Google Scholar 
Wright, E. The History of the European Aurochs (Bos primigenius) from the Middle Pleistocene to Its Extinction: An Archaeological Investigation of Its Evolution, Morphological Variability and Response to Human Exploitation. (PhD. Thesis, University of Sheffield, 2013).Koenigswald, W. V., Sander, P. M. & Walders, M. The Upper Pleistocene tracksite Bottrop-Welheim (Germany). Acta Zool. Cracov. 39(1), 235–244 (1996).
Google Scholar 
Martínez-Navarro, B., Rook, L., Papini, M. & Libsekal, Y. A new species of bull from the Early Pleistocene paleoanthropological site of Buia (Eritrea): Parallelism on the dispersal of the genus Bos and the Acheulian culture. Quat. Intern. 212(2), 169–175. https://doi.org/10.1016/j.quaint.2009.09.003 (2010).Article 

Google Scholar 
Van Vuure, C. Retracing the Aurochs: History, Morphology and Ecology of an Extinct Ox (Coronet Books, 2005).
Google Scholar 
Franks, J. W. Interglacial deposits at Trafalgar Square, London. N. Phytologist 59(2), 145–152 (1960).Article 

Google Scholar 
Estévez, J. & Saña, M. Auerochsenfunde auf der Iberischen Halbinsel. in Archäologie und Biologie des Auerochsen (ed. Weniger, G.-C.) (Neanderthal Museum, 1999).Mona, S. et al. Population dynamic of the extinct European aurochs: Genetic evidence of a north-south differentiation pattern and no evidence of post-glacial expansion. BMC Evol. Biol. 10, 1–13 (2010).Article 
CAS 

Google Scholar 
Rodríguez-Vidal, J. et al. Undrowning a lost world—The Marine isotope stage 3 landscape of Gibraltar. Geomorphology 203, 105–114 (2013).ADS 
Article 

Google Scholar 
Pfeiffer, T. Systematic relationship between the Bovini with special references to the fossil taxa Bos primigenius Bojanus and Bison priscus Bojanus. in Archäologie und Biologie des Auerochsen (ed. Weniger, G.-C.). 59–70. (Neanderthal Museum, 1999).Zazula, G. D. et al. A late Pleistocene steppe bison (Bison priscus) partial carcass from Tsiigehtchic, Northwest Territories, Canada. Quat. Sci. Rev. 28(25–26), 2734–2742 (2009).ADS 
Article 

Google Scholar 
Boeskorov, G. G. et al. The Yukagir Bison: The exterior morphology of a complete frozen mummy of the extinct steppe bison, Bison priscus from the early Holocene of northern Yakutia, Russia. Quat. Intern. 406, 94–110. https://doi.org/10.1016/j.quaint.2015.11.084 (2016).Article 

Google Scholar 
Ekström, J. The Late Quaternary History of the Urus (Bos primigenius Bojanus 1827) in Sweden. PhD. Thesis. (Lund University, 1993).Grange, T. et al. The evolution and population diversity of Bison in Pleistocene and Holocene Eurasia: Sex matters. Diversity 10(3), 65. https://doi.org/10.3390/d10030065 (2018).Article 

Google Scholar 
Castaños, J., Castaños, P. & Murelaga, X. First complete skull of a Late Pleistocene Steppe Bison (Bison priscus) in the Iberian Peninsula. Ameghiniana 53(5), 543–551. https://doi.org/10.5710/amgh.03.06.2016.2995 (2016).Article 

Google Scholar 
Álvarez-Lao, D. J., Kahlke, R.-D., García, N. & Mol, D. The Padul mammoth finds: On the southernmost record of Mammuthus primigenius in Europe and its southern spread during the Late Pleistocene. Palaeogeogr. Palaeocl. Palaeoecol. 278(1–4), 57–70 (2009).ADS 
Article 

Google Scholar 
Loope, D. B. Recognizing and utilizing vertebrate tracks in cross section: Cenozoic hoofprints from Nebraska. Palaios 1, 141–151 (1986).ADS 
Article 

Google Scholar 
Albarella, U., Dobney, K. & Rowley-Conwy, P. Size and shape of the Eurasian wild boar (Sus scrofa), with a view to the reconstruction of its Holocene history. Environ. Archaeol. 14, 103–136 (2009).Article 

Google Scholar 
Davis, S. J. M. The effects of temperature change and domestication on the body size of Late Pleistocene to Holocene mammals of Israel. Palaeobiology 7, 101–114 (1981).Article 

Google Scholar 
Cerilli, E. & Petronio, C. Biometrical variations of Bos primigenius Bojanus 1827 from middle Pleistocene to Holocene. in Proceedings of the International Symposium on ‘Ongulés/Ungulates’, Toulouse. 37–42. (1991).Davis, S. J. M. & Mataloto, R. Animal remains from Chalcolithic of São Pedro (Redondo, Alentejo): Evidence for a crisis in the Mesolithic. Rev. Port. Arqueol. 15, 47–85 (2012).
Google Scholar 
Mariezkurrena, K. & Altuna, J. Biometría y diformismo sexual en el esqueleto de Cervus elaphus würmiense, postwürmiense y actual del Cantábrico. Munibe (Antr.-Arkeol.) 35, 203–246 (1983).
Google Scholar 
Davis, S. J. M. The mammals and birds from the Gruta do Caldeirão, Portugal. Rev. Port. Arqueol. 5, 29–98 (2002).CAS 

Google Scholar 
Barr, K. Prehistoric Avian, Mammalian and H. sapiens Footprint—Tracks from Intertidal Sediments as Evidence of Human Palaeoecology. PhD. Thesis. (University of Reading, 2018).Hall, J. G. A comparative analysis of the habitat of the extinct aurochs and other prehistoric mammals in Britain. Ecography 31, 187–190 (2008).Article 

Google Scholar 
Bicho, N. F., Gibaja, J. F., Stiner, M. & Manne, T. L. Paléolithique supérieur au sud du Portugal: Le site du Vale do Boi. L’antropologie 114, 48–67 (2010).
Google Scholar 
Bicho, N. & Haws, J. The Magdelian in central and southern Portugal: Human ecology at the end of the Pleistocene. Quatern. Int. 272–273, 6–16 (2012).Article 

Google Scholar 
Cortés-Sánchez, M. et al. Palaeoenvironmental and cultural dynamics of the coast of Málaga (Andalusia, Spain) during the Upper Pleistocene and early Holocene. Quatern. Sci. Rev. 27, 2176–2193 (2008).ADS 
Article 

Google Scholar 
Bohórquez, A. M., Ruiz, C. B., Caparrós, M. & Moigne, A. M. Una aproximación a la compreensión de la fauna de macromamiferos de la Cueva de Zafarraya (Alcaucín, Málaga). Menga Rev. Prehist. Andalucía 3, 83–105 (2012).
Google Scholar 
Ripoll, M. P. & Maroto, J. L. fauna mediterránea durante el Pleistoceno superior del Mediterráneo Ibérico. Kobie Serie Anejo 18, 27–38 (2021).
Google Scholar 
Lazo, A. Ranging behaviour of feral cattle (Bos taurus) in Doñana National Park, S.W. Spain. J. Zool. 236(3), 359–369. https://doi.org/10.1111/j.1469-7998.1995.tb02718.x (1995).Article 

Google Scholar 
AliceVision. Meshroom: V2021.1.0. GNU-GPL. https://alicevision.org/ (2020).OpenDroneMap Authors ODM. A Command Line Toolkit to Generate Maps, Point Clouds, 3D Models and DEMs from Drone, Balloon or Kite Images. OpenDroneMap/ODM GitHub Page. https://github.com/OpenDroneMap/WebODM (2020).Cignoni, P., Callieri, M., Corsini, M., Dellepiane, M., Ganovelli, F. & Ranzuglia, G. MeshLab: an open-source mesh processing tool. in Sixth Eurographics Italian Chapter Conference. 129–136. MeshLab V. 2020.12. https://www.meshlab.net/ (2008).CloudCompare. V2.11.0. GNU-GPL. https://www.cloudcompare.org (2020).Zhukov, S., Iones, A. & Kronin, G. An ambient light illumination model. Render. Tech. 98, 45–55 (1998).Article 

Google Scholar 
Vergne, R., Pacanowski, R., Barla, P., Granier, X., & Schlick, C. Radiance scaling for versatile surface enhancement. in Proceedings of the 2010 ACMSIGGRAPH Symposium on Interactive 3D Graphics and Games.143–150. (2010). More

Genome characteristics of ancient obligate symbiontsWe first tested the hypothesis that each of the ant lineages sequenced in our study (Cardiocondyla, Formica, and Plagiolepis) hosts its own ancient strictly vertically transmitted symbiont that have co-speciated with its host, which has been shown previously in the Camponotus- Blochmannia symbiosis [17]. To address this aim, we compared the genomes of symbionts from 13 species of ants, 8 from our study combined with 5 previously published genomes, representing four independently evolved symbioses. This includes symbionts from three Formica, two Plagiolepis, and an additional three Cardiocondyla species that we sequenced, in addition to four previously published genomes from Blochmannia, the obligate symbiont of Camponotus ants, and the one pre-existing Westeberhardia genome from Cardiocondyla obscurior [8, 18,19,20,21].We found the gene order of single copy orthologs in symbionts is highly conserved in ant species belonging to the same genus (Fig. 1). This type of structural stability of genomes is typically found in symbionts that have been strictly vertically transmitted within a matriline [22] and has been documented in the obligate symbionts of whiteflies, psyllids, cockroaches, and aphids [23,24,25,26]. In contrast, genome structure differed substantially between symbionts from different ant genera (Fig. 1, Fig. S1). We also find that the host and symbiont phylogenies are in general concordance in Cardiocondyla (TreeMap: p = 0.00100 CI95% = [0.00000, 0.00424]), and in Formica the topologies suggest co-segregation, although there were too few nodes to confirm this statistically (Fig. S2). Together, this strongly suggests the symbioses in all four ant lineages are independently acquired ancient associations that have co-speciated with their hosts.Fig. 1: Structural stability of ant symbiont genomes.A Ant lineages known to host bacteriocyte-associated symbionts (red font) and lineages not known to (black font), based on [91]. Outgroup (grey font) not examined in this study. B Visualisation of symbiont genomes showing conservation of gene order in the symbionts of ant species that belong to the same genus. Blocks show the locations of single copy orthologs in the symbiont genome, lines connect shared single copy orthologs between genomes. All genomes and annotations were generated in this study except the Blochmannia symbionts and the Westeberhardia strain from C. obscurior [8, 18,19,20,21]. *Evidence of symbionts were detected in embryos of Anoplolepis [91] but it is unclear if they are localised in bacteriocytes in larvae and adults.Full size imageIn addition, our phylogenetic analysis reveals that all four symbiont lineages originate from a single clade, the Sodalis-allied bacteria (Fig. 2). This demonstrates that ant lineages that host bacteriocytes-associated symbionts have convergently acquired related bacteria, which differs from previous findings based on limited taxa and genes [27]. All of the symbionts have evidence of advanced genome reduction, which is characterized by reduced genome size, GC content, and number of coding sequences, similar to other ancient obligate symbionts of insects [4]. The three strains of Westeberhardia we analysed have extremely small (0.45–0.53 Mb) GC depleted genomes (22–26%) that are similar to the figures reported for the strain in Cardiocondyla obscurior [8]; confirming that they have some of the smallest genomes of any known gammaproteobacterial endosymbiont (Fig. 2). By comparison, the symbionts in Formica and Plagiolepis have genomes around twice the size (1.37–1.38 Mb) and GC content (~41%) of Westeberhardia (Fig. 2) raising the possibility that they are in an earlier stage of genome reduction than both Westeberhardia and Blochmannia. The Formica and Plagiolepis symbionts have a similar size, GC range, and number of coding sequences as known obligate symbionts such as Candidatus Doolittlea endobia [28], and several Serratia symbiotica lineages that are co-obligate symbionts in aphids [29].Fig. 2: Phylogenetic origins of the bacteriocyte-associated symbionts of ants.A pruned phylogeny of gammaproteobacterial endosymbionts based on Fig. S8. The phylogeny is based on a dayhoff6 recoded amino acid alignment of 72 genes analysed using phylobayes. Bar plots represent the size (in Mbp) and GC content of symbiont genomes. Bars are colour coded to represent hypothesised relationships between symbionts and hosts. Species names highlighted in red in the phylogeny indicate the four bacteriocyte-associated symbionts of ants. Genomes sequenced and assembled for this paper are referenced as ‘novel symbiont’ lineages. Full phylogenies with node support and branch lengths are available as Fig. S8 and Fig. S9, respectively.Full size imageBacteriocyte-associated endosymbiontsUsing fluorescent in situ hybridisation, we determine whether the Sodalis-allied symbionts we sequenced are localised in bacteriocytes to confirm they are the associations first observed by Lillienstern and Jungen in the early 1900’s [10, 11].Consistent with Lilienstern’s findings [11], we found the Sodalis symbiont in Formica ants is distributed in bacteriocytes surrounding the midgut in adult queens (Fig. 3A). The symbionts are also found in eggs and ovaries of adult queens, indicating they are vertically transmitted from queens to offspring (Fig. 3B–C). Sectioning of F. cinerea larvae shows the bacteriocytes to be arranged in a single layer of cells surrounding the midgut, as well as in clusters of bacteriocytes closely situated to the midgut (Fig. 3D–D’). In adult Plagiolepis queens, the symbiont was not present in bacteriocytes around the midgut, suggesting the symbiont may play a more substantive role in larval development or pupation and then migrates to the ovaries prior to or during metamorphosis. Apart from that, the localisation of the symbiont in Plagiolepis was the same as in Formica – symbionts in larval midgut bacteriocytes, ovaries and eggs (Fig. S3) – supporting Jungen’s cytological findings [10]. Bacteriocytes are also found surrounding the midgut in Camponotus and Cardiocondyla ants [8, 30, 31] indicating the symbionts are localised in a similar manner in all four ant lineages.Fig. 3: Anatomical localisation of symbiont in Formica ants.Fluorescent in situ hybridisation (FISH) generated images showing the localisation of symbionts in Formica ants. A–C Whole mount FISH of Formica fusca: queen gut (A, crop and proventriculus on the right, midgut in the middle, hindgut and Malpighian tubules on the left), ovaries (B) and egg (C). DAPI staining of host tissue in blue, symbiont stained in red. D–D’. FISH on transverse cytological sections of Formica cinerea larva midgut. DAPI staining only, showing host nuclei of bacteriocytes in a single layer surrounding the midgut (D), and a magnified region highlighting symbionts in red localised within bacteriocytes and in a bacteriome (D’). A FISH image of the symbiont-free midgut of a Formica lemani queen is available as Fig. S11.Full size imageConservation of metabolic functions in ant endosymbiontsDespite on-going genome reduction, obligate symbionts of insects typically retain gene networks required for maintaining the symbiosis with their host, such as pathways for synthesising essential nutrients. This has resulted in the symbionts of sap- and blood-feeding insects converging on genomes that have retained the same sets of metabolic pathways – to synthesise essential nutrients missing in their hosts’ diets [32, 33]. Here we compare the metabolic pathways retained in the reduced genomes of the four bacteriocyte-associated symbionts of ants to test the hypothesis that have been acquired to perform similar functions. For this, we assess whether they have consistently retained metabolic pathways to synthesise the same key nutrients. Two major patterns stand out.The first major pattern we find is that the four ant symbionts have all retained the shikimate pathway, which produces chorismate, along with most of the steps necessary to produce tyrosine from this precursor (Tables 1 and S2). Both the symbiont of Formica and Westeberhardia each lack one of the genes required to produce tyrosine. However, in Westeberhardia it is believed the host encodes the missing gene, supplying the enzyme to fulfil the final step of the pathway [8]. Intriguingly, we find that this gene is also present in the Formica ant genomes (Fig. S4). In addition, all symbionts except Westeberhardia can produce phenylalanine which is a precursor that can be converted to tyrosine by their hosts [5, 34, 35]. Tyrosine is important for insect development as it is used to produce L-DOPA, which is a key component of insect cuticles [5]. Tyrosine is also a precursor for melanin synthesis, which is important in protection against pathogens, and plays a fundamental role in neurotransmitters and hormone production [36, 37]. In several species of ants, weevils, and other beetles, symbionts are believed to provision hosts with tyrosine, and it has been shown experimentally in several of these species that removal or inhibition of their symbionts causes cuticle development to suffer [38,39,40,41,42,43,44,45,46,47]. A thicker cuticle has been shown to help symbiont-carrying grain beetles resist desiccation [43], and defend against natural enemies [48]. However, female reproduction is delayed at higher humidity, suggesting a metabolic cost to carrying their Bacteroidetes symbiont. Tyrosine provisioning is also the likely function of Westeberhardia in Cardiocondyla ants, as this is one of the few nutrient pathways retained in this symbiont. Our analysis confirms the shikimate pathway, and the symbiont portions of the tyrosine pathway, have been retained in Westeberhardia from three phylogenetically diverse Cardiocondyla lineages, providing additional support for this hypothesis. In addition to tyrosine, most of the symbionts have retained the capacity to produce vitamin B9 (tetrahydrofolate) and all can perform the single step conversions necessary to produce alanine and glycine. However, our gene enrichment analysis indicates that tyrosine, and the associated chorismate biosynthetic process, are the only enriched vitamin or amino acid pathways that are shared by all of the symbiont genomes (Table S1). This suggests that provisioning of tyrosine by symbionts, or tyrosine precursors, is of general importance across all bacteriocyte-associated symbioses of ants.Table 1 Comparison of the retention and losses of metabolic pathways for key nutrients across ant symbionts.Full size tableThe second major pattern emerging from our comparative analysis is that there are clear differences in the pathways lost or retained across symbionts (Tables 1 and S2). This is most evident when comparing Blochmannia with Westeberhardia, the latter of which has lost the capacity to synthesise most essential nutrients. The symbionts of Formica or Plagiolepis, in contrast, have retained the capacity to synthesise many of the same amino acids and B vitamins as Blochmannia, suggesting they may perform similar functions for their hosts. However, Blochmannia has retained more biosynthetic pathways, particularly those involved in the synthesis of essential amino acids. Previous experimental studies have confirmed that Blochmannia provisions hosts with essential amino acids [1]. The absence of several core essential amino acids in the Formica and Plagiolepis symbionts may reflect differences in the dietary ecology of the different ant genera. The retention of the full complement of essential amino acids biosynthetic pathways in the highly reduced genome of Blochmannia does however indicate it plays a more substantive nutrient-provisioning role for its hosts than the other ant symbionts we investigated.Previous work on the extracellular gut symbionts of several arboreal ant lineages identified nitrogen recycling via the urease operon as a function that may be of key importance for ant symbioses [1, 2, 49, 50]. However, we do not find any evidence that the symbionts of Formica, Plagiolepis, or Cardiocondyla play a role in nitrogen recycling via the urease operon (Table 1). This suggests that nitrogen recycling may play an important role for more strictly herbivorous ants, such as Cephalotes. Our results indicate tyrosine supplementation by symbionts may be universally required for essential physiological process across a broader range of ant lineages.The origins and losses of symbioses in Formica and Cardiocondyla
We investigated the presence of the symbiont in phylogenetically diverse Formica and Cardiocondyla species to identify the evolutionary origins and losses of the symbiosis. Although the symbiont in Plagiolepis was present in P. pygmaea and two unknown Plagiolepis species we investigated, we did not have sufficient phylogenetic sampling to assess the origins of the symbiosis.In Formica, we find the symbiont is restricted to a single clade in the paraphyletic Serviformica group (Fig. 4A). The species in this clade are socially polymorphic, forming both multi-queen and single-queen colonies [51]. Based on a previously dated phylogeny of Formica ants, we estimate the symbiosis originated approximately 12–22 million years ago [52]. In Cardiocondyla, the symbiosis is widespread throughout the genus. The prevalence of the symbiont in Cardiocondyla, in combination with its highly reduced genome, suggests it is a very old association that likely dates back to the origins of the ant genus some 50–75 million years ago [53]. The symbiont was also absent in two clades, the argentea and palearctic groups (Fig. 4B). This may represent true evolutionary losses in these clades. It may be that these losses are linked to a notable change in social structure in these two Cardiocondyla clades, having gone from the ancestral state of maintaining multi-queen colonies to single-queen colonies [54], however it is not clear how this could impact the symbiosis.Fig. 4: Phylogenetic distribution of symbionts in queens of Formica and Cardiocondyla ants.Pie charts represent the proportion of Formica (A) and Cardiocondyla (B) queens sampled that carried the symbiont (red) and those that did not (grey). Numbers represent the number of queens positive for the symbiont over the total number of queens sampled (intracolony infection frequencies in Table S5). See the supplementary material for the statistical testing of differences in prevalence within Serviformica Clade 1. The Formica phylogeny is based on [81] and the Cardiocondyla phylogeny is based on [83], with major clades highlighted. Dashed lines indicate species added to the original source phylogeny based on additional published phylogenies (specified in the Taxonomic Analysis section of the methods). Starred names are provisional names of a recognised morphospecies to be described by B. Seifert.Full size imageEvidence of variation in colony-level dependence on symbiontsObservations from individual studies on F. cinerea and F. lemani [10, 11], as well as Cardiocondyla obscurior [8], reported rare cases of ant queens not harbouring their symbionts in nature. This called into question the degree to which these insects depend on symbionts for nutrients, and whether the symbiosis may be breaking down in certain host lineages. However, given the limited number of species and populations studied, it is unclear how often colonies are maintained with uninfected queens, and whether this varies across species, suggesting species may differ in their dependence on their symbiont. To answer this question, we assessed the presence of the symbionts in 838 samples from 147 colonies of phylogenetically diverse Formica and Cardiocondyla species collected across 8 countries.Our investigation reveals the natural occurrence of uninfected queens is a widespread phenomenon in many Formica and Cardiocondyla species (Fig. 4). We confirmed the absence of symbionts in queens, and that they have not been replaced with another bacterial or fungal symbiont, using multiple approaches including diagnostic PCR, metagenomic and deep-coverage amplicon sequencing (Tables S3,  S4, Figs. S5, S6). Wolbachia was high in relative abundance, especially in Formica ants, but was not sufficiently present across samples to be a feasible replacement. There was also clear evidence of variation across host species. In Formica, queens and workers of F. fusca always carried the symbiont, whereas queens and workers of F. lemani, F. cinerea, and F. selysi showed varying degrees of individuals not carrying the symbionts (Fig. 4A, Table S5). A similar pattern can be seen in Cardiocondyla, where queens of several species, such as C. obscurior, always carry the symbiont, compared to lower incidences in other species (Fig. 4B). Klein et al [8] identified a single C. obscurior colony with uninfected queens in Japan. However, queens of this species nearly always carry the symbiont in nature.The degradation and eventual loss of symbionts from bacteriocytes has been reported in males, and in sterile castes of aphids and ants [55], which do not transmit symbionts to offspring. In reproductive females, bacteriocytes may degrade as a female ages; however, symbionts are typically retained at high bacterial loads in the ovaries, as this is required to maintain the symbionts within the germline [31]. All of the symbiotic ant species we investigated maintain multi-queen colonies, and the vast majority had at least one queen, often more, within a colony that carried the symbiont (Table S5). We hypothesize that species that maintain colonies with uninfected queens may be able to retain sufficient colony-level fitness with only a fraction of queens harbouring the symbiont and receiving its nutritive benefits.Dependence on symbionts in a socioecological contextThe retention of symbionts in queens and workers of some species, but not others, suggests species either differ in their dependence on symbiont-derived nutrients, or that symbionts have lost the capacity to make nutrients in certain host lineages. Our analysis of symbiont genomes did not reveal any structural differences, such as the disruption of metabolic pathways, which could explain differences in symbiont retention between host species (Table S2). This suggests differences in the retention of symbionts may reflect differences in host ecologies.In ants, which occupy a wide range of feeding niches, reliance on symbiont-derived nutrients will largely depend on lineage-specific feeding ecologies. For example, several species of arboreal Camponotus ants have been shown to be predominantly herbivorous [56]. Blochmannia, in turn, has retained the capacity to synthesise key nutrients lacking in their plant-based diets, such as essential amino acids [1]. Blochmannia is also always present in queens and workers [31], which is a testament to the importance of these nutrients for the survival of its primarily herbivorous host [13]. In contrast, Formica and Cardiocondyla species are thought to have a more varied diet [14]. Diet flexibility and altered foraging efforts may therefore reduce their reliance on a limited number of symbiont-derived nutrients allowing colonies of some species to persist with uninfected queens in certain contexts. Silvanid beetles and grain weevils, for example, can survive in the absence of their tyrosine-provisioning symbionts [38, 57, 58] when provided nutritionally balanced diets, in the laboratory [57] or in cereal grain elevators [59, 60]. Similarly, studies on Cardiocondyla and Camponotus ants have shown they can maintain sufficient colony health in the absence of their symbionts, if provided a balanced diet [31, 61]. It would be interesting to know whether species of Formica and Cardiocondyla that always carry the symbiont in nature, such as F. fusca and C. obscurior, have more restricted diets with less access to nutrients such as tyrosine, as this may explain their dependence on their symbiont for nutrients and tendency to harbour them in queens.Although it is unusual for bacteriocyte-associated symbionts to be absent in reproductive females, the fact that it is simultaneously occurring in phylogenetically diverse species from many locations suggests the symbiosis may have persisted in this manner over evolutionary time. Perhaps through diet flexibility colonies can be maintained with uninfected queens in some contexts, however we expect them to be disadvantaged in other ecological scenarios. Fluctuating environmental conditions may therefore eventually purge asymbiotic queens from lineages, allowing the symbiosis to be retained over longer periods of evolutionary time. The multiple-queen colony lifestyle in all symbiotic Formica and Cardiocondyla species we investigated may also provide an additional social buffer that limits the costs to individual queens being asymbiotic. Workers will still nourish larvae and queens without symbionts and colony fitness may be maintained through the reproductive output of nestmate queens that carry the symbiont. There may also be an adaptive explanation for the losses if, for example, metabolic costs to maintain the symbiosis trade off in a context dependent manner [44, 62, 63]. Under this scenario, maintaining a mix of infected and uninfected queens may benefit a colony by allowing for optimal reproduction under a broader range of environmental scenarios.Our data suggest that symbiotic relationships can evolve to solve common problems but also rapidly break down if the symbiosis is no longer required, or potentially when costs are too high [44]. We have identified tyrosine provisioning as a possible unifying function across bacteriocyte-associated symbionts of ants. But we have also shown species can vary in how much they depend on symbionts for nutrients. Our results demonstrate that ants have a unique labile symbiotic system, allowing us to better understand the evolutionary forces that influence the persistence and breakdown of long-term endosymbiotic mutualisms.
Candidatus Liliensternia hugann and Candidatus Jungenella plagiolepisWe propose the names Candidatus Liliensternia hugann for the Sodalis-allied symbiont found in Formica. The genus name is in honour of Margarete Lilienstern who first identified the symbiont [11]. The species name is derived from the combined first names of the first authors parents. Similarly, we propose the name of Candidatus Jungenella plagiolepis for the Plagiolepis-bound symbiont. The genus name is in honour of Hans Jungen who originally discovered the symbiont [10], and the species name is derived from Plagiolepis, the genus in which the symbiont can be found. More

Zaiss, M. M. & Harris, N. L. Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol. 38, 5–11 (2016).CAS 
PubMed 
Article 

Google Scholar 
Jhan, K. Y. et al. Angiostrongylus cantonensis causes cognitive impairments in heavily infected BALB/c and C57BL/6 mice. Parasites Vectors. 13, 405. https://doi.org/10.1186/s13071-020-04230-y (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Boillat, M. et al. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasma gondii. Cell Rep. 30, 320–334 (2020).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Brombacher, T. M. et al. Nippostrongylus brasiliensis infection leads to impaired reference memory and myeloid cell interference. Sci. Rep. 8, 2958. https://doi.org/10.1038/s41598-018-20770-x (2018).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Kavaliers, M. & Colwell, D. D. Reduced spatial learning in mice infected with the nematode Heligmosomoides polygyrus. Parasitology 110(Pt 5), 591–597 (1995).PubMed 
Article 

Google Scholar 
Pan, S. C. et al. Cognitive and microbiome impacts of experimental Ancylostoma ceylanicum hookworm infections in hamsters. Sci. Rep. 9, 7868. https://doi.org/10.1038/s41598-019-44301-4 (2019).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Blecharz-Klin, K. et al. Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters. PLoS Pathog. 18, e1010330–e1010330. https://doi.org/10.1371/journal.ppat.1010330 (2022).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Braithwaite, V. et al. Spatial and discrimination learning in rodents infected with the nematode Strongyloides ratti. Parasitology 117(Pt 2), 145–154 (1998).PubMed 
Article 

Google Scholar 
Sharma, S., Rakoczy, S. & Brown-Borg, H. Assessment of spatial memory in mice. Life Sci. 87, 521–536 (2010).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Vorhees, C. V. & Williams, M. T. Assessing spatial learning and memory in rodents. ILAR J. 55, 310–332 (2014).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Pelletier, F., Page, K. A., Ostiguy, T. & Festa-Bianchet, M. Fecal counts of lungworm larvae and reproductive effort in bighorn sheep. Ovis canadensis. Oikos. 110, 473–480 (2005).Article 

Google Scholar 
Odiere, M. R., Koski, K. G., Weiler, H. A. & Scott, M. E. Concurrent nematode infection and pregnancy induce physiological responses that impair linear growth in the murine foetus. Parasitology 137, 991–1002 (2010).CAS 
PubMed 
Article 

Google Scholar 
Fitzgerald, E., Hor, K. & Drake, A. J. Maternal influences on fetal brain development: The role of nutrition, infection and stress, and the potential for intergenerational consequences. Early Hum. Dev. 150, 105190. https://doi.org/10.1016/j.earlhumdev.2020.105190 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Boksa, P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24, 881–897 (2010).PubMed 
Article 

Google Scholar 
Akitake, Y. et al. Moderate maternal food restriction in mice impairs physical growth, behavior, and neurodevelopment of offspring. Nutr. Res. 35, 76–87 (2015).CAS 
PubMed 
Article 

Google Scholar 
Hammelrath, L. et al. Morphological maturation of the mouse brain: An in vivo MRI and histology investigation. Neuroimage 125, 144–152 (2016).PubMed 
Article 

Google Scholar 
Wills, T., Muessig, L. & Cacucci, F. The development of spatial behaviour and the hippocampal neural representation of space. Philos. Trans. R. Soc. B: Biol. Sci. 369, 20130409. https://doi.org/10.1098/rstb.2013.0409 (2014).Article 

Google Scholar 
Travaglia, A., Steinmetz, A. B., Miranda, J. M. & Alberini, C. M. Mechanisms of critical period in the hippocampus underlie object location learning and memory in infant rats. Learn Mem. 25, 176–182 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
McHail, D. G., Valibeigi, N. & Dumas, T. C. A Barnes maze for juvenile rats delineates the emergence of spatial navigation ability. Learn Mem. 25, 138–146 (2018).PubMed 
PubMed Central 
Article 

Google Scholar 
Bliss, T. V. P., Collingridge, G. L., Morris, R. G. M. & Reymann, K. G. Long-term potentiation in the hippocampus: Discovery, mechanisms and function. Neuroforum 24, A103–A120 (2018).Article 

Google Scholar 
Schiller, D. et al. Memory and space: Towards an understanding of the cognitive map. J. Neurosci. 35, 13904–13911 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Kim, J. J. & Diamond, D. M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453–462 (2002).CAS 
PubMed 
Article 

Google Scholar 
Jiang, P. et al. The persistent effects of maternal infection on the offspring’s cognitive performance and rates of hippocampal neurogenesis. Prog. Neuropsychopharmacol. Biol. Psychiatry. 44, 279–289 (2013).CAS 
PubMed 
Article 

Google Scholar 
Wallace, K. L. et al. Interleukin-10/Ceftriaxone prevents E. coli-induced delays in sensorimotor task learning and spatial memory in neonatal and adult Sprague-Dawley rats. Brain. Res. Bull. 81, 141–148 (2010).Shi, L., Fatemi, S. H., Sidwell, R. W. & Patterson, P. H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23, 297–302 (2003).PubMed 
PubMed Central 
Article 

Google Scholar 
Denenberg, V. H. Open-field behavior in the rat: what does it mean?. Ann. N. Y. Acad. Sci. 159, 852–859 (1969).ADS 
CAS 
PubMed 
Article 

Google Scholar 
Vogel-Ciernia, A. & Wood, M. A. Examining object location and object recognition memory in mice. Curr. Protoc. Neurosci. 69, 8.31.1–17 (2014).Denninger, J. K., Smith, B. M. & Kirby, E. D. Novel object recognition and object location behavioral testing in mice on a budget. J. Vis. Exp. https://doi.org/10.3791/58593 (2018).Article 
PubMed 

Google Scholar 
Krüger, H.-S., Brockmann, M. D., Salamon, J., Ittrich, H. & Hanganu-Opatz, I. L. Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats. Neurobiol. Learn. Mem. 97, 470–481 (2012).PubMed 
Article 

Google Scholar 
Cruz-Sanchez, A. et al. Developmental onset distinguishes three types of spontaneous recognition memory in mice. Sci. Rep. 10, 10612. https://doi.org/10.1038/s41598-020-67619-w (2020).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Sunyer, B., Patil, S., Hoger, H. & Lubec, G. Barnes maze, a useful task to assess spatial reference memory in the mice. Nat. Protoc. https://doi.org/10.1038/nprot.2007.390 (2007).Article 

Google Scholar 
Schenk, F. Development of place navigation in rats from weaning to puberty. Behav. Neural Biol. 43, 69–85 (1985).CAS 
PubMed 
Article 

Google Scholar 
Brown, R. W. & Kraemer, P. J. Ontogenetic differences in retention of spatial learning tested with the Morris water maze. Dev. Psychobiol. 30, 329–341 (1997).CAS 
PubMed 
Article 

Google Scholar 
Batinić, B. et al. Lipopolysaccharide exposure during late embryogenesis results in diminished locomotor activity and amphetamine response in females and spatial cognition impairment in males in adult, but not adolescent rat offspring. Behav. Brain Res. 299, 72–80 (2016).PubMed 
Article 
CAS 

Google Scholar 
Lante, F. et al. Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain. Free Radic. Biol. Med. 42, 1231–1245 (2007).CAS 
PubMed 
Article 

Google Scholar 
Wang, H. et al. Age- and gender-dependent impairments of neurobehaviors in mice whose mothers were exposed to lipopolysaccharide during pregnancy. Toxicol. Lett. 192, 245–251 (2010).CAS 
PubMed 
Article 

Google Scholar 
Yagi, S. & Galea, L. A. M. Sex differences in hippocampal cognition and neurogenesis. Neuropsychopharmacology 44, 200–213 (2019).PubMed 
Article 

Google Scholar 
Vuoksimaa, E. et al. Brain structure mediates the association between height and cognitive ability. Brain Struct. Func. 223, 3487–3494 (2018).Article 

Google Scholar 
Harris, M. A., Brett, C. E., Deary, I. J. & Starr, J. M. Associations among height, body mass index and intelligence from age 11 to age 78 years. BMC Geriatr. 16, 167. https://doi.org/10.1186/s12877-016-0340-0 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Pereira, V. H. et al. Adult body height is a good predictor of different dimensions of cognitive function in aged individuals: A cross-sectional study. Front. Aging Neurosci. 8, 1. https://doi.org/10.3389/fnagi.2016.00217 (2016).Case, A. & Paxson, C. Stature and status: Height, ability, and labor market outcomes. J. Polit. Econ. 116, 499–532 (2008).PubMed 
PubMed Central 
Article 

Google Scholar 
Frick, K. M., Kim, J., Tuscher, J. J. & Fortress, A. M. Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents. Learn Mem. 22, 472–493 (2015).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Qiu, L. R. et al. Mouse MRI shows brain areas relatively larger in males emerge before those larger in females. Nat. Commun. 9, 2615. https://doi.org/10.1038/s41467-018-04921-2 (2018).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Towe, A. L. & Mann, M. D. Brain size/body length relations among myomorph rodents. Brain Behav. Evol. 39, 17–23 (1992).CAS 
PubMed 
Article 

Google Scholar 
Perepelkina, O. V., Tarasova, A. Y., Ogienko, N. A., Lil’p, I. G. & Poletaeva, I. I. Brain weight and cognitive abilities of laboratory mice. Biol. Bull. Rev. 10, 91–101 (2020).Odiere, M. R., Scott, M. E., Weiler, H. A. & Koski, K. G. Protein deficiency and nematode infection during pregnancy and lactation reduce maternal bone mineralization and neonatal linear growth in mice. J. Nutr. 140, 1638–1645 (2010).CAS 
PubMed 
Article 

Google Scholar 
Sánchez, M. B. et al. Leishmania amazonensis infection impairs reproductive and fetal parameters in female mice. Rev. Argent. Microbiol. 53, 194–201 (2021).PubMed 

Google Scholar 
Haque, M., Koski, K. G. & Scott, M. E. Maternal gastrointestinal nematode infection up-regulates expression of genes associated with long-term potentiation in perinatal brains of uninfected developing pups. Sci. Rep. 9, 4165. https://doi.org/10.1038/s41598-019-40729-w (2019).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Gregory, R. D., Montgomery, S. S. J. & Montgomery, W. I. Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. J. Anim. Ecol. 61, 749–757 (1992).Article 

Google Scholar 
Reynolds, L. A., Filbey, K. J. & Maizels, R. M. Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin. Immunopathol. 34, 829–846 (2012).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Maizels, R. M. et al. Immune modulation and modulators in Heligmosomoides polygyrus infection. Exp. Parasitol. 132, 76–89 (2012).CAS 
PubMed 
Article 

Google Scholar 
Haque, M., Starr, L. M., Koski, K. G. & Scott, M. E. Differential expression of genes in fetal brain as a consequence of maternal protein deficiency and nematode infection. Int. J. Parasitol. 48, 51–58 (2018).CAS 
PubMed 
Article 

Google Scholar 
Hsueh, P.-T. et al. Immune imbalance of global gene expression, and cytokine, chemokine and selectin levels in the brains of offspring with social deficits via maternal immune activation. Genes Brain Behav. 17, e12479. https://doi.org/10.1111/gbb.12479 (2018).Steimer, T. The biology of fear- and anxiety-related behaviors. Dialogues Clin. Neurosci. 4, 231–249 (2002).PubMed 
PubMed Central 
Article 

Google Scholar 
Ricceri, L., Colozza, C. & Calamandrei, G. Ontogeny of spatial discrimination in mice: A longitudinal analysis in the modified open-field with objects. Dev. Psychobiol. 37, 109–118 (2000).CAS 
PubMed 
Article 

Google Scholar 
Howland, J. G., Cazakoff, B. N. & Zhang, Y. Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 201, 184–198 (2012).CAS 
PubMed 
Article 

Google Scholar 
Ito, H. T., Smith, S. E. P., Hsiao, E. & Patterson, P. H. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav. Immun. 24, 930–941 (2010).PubMed 
PubMed Central 
Article 

Google Scholar 
Meyer, U. et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 26, 4752–4762 (2006).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Meyer, U. et al. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol. Psychiatry. 13, 208–221 (2008).CAS 
PubMed 
Article 

Google Scholar 
Chapillon, P. & Roullet, P. Use of proximal and distal cues in place navigation by mice changes during ontogeny. Dev. Psychobiol. 29, 529–545 (1996).CAS 
PubMed 
Article 

Google Scholar 
Variyam, E. P. & Banwell, J. G. Hookworm disease: Nutritional implications. Rev. Infect. Dis. 4, 830–835 (1982).CAS 
PubMed 
Article 

Google Scholar 
Bansemir, A. D. & Sukhdeo, M. V. The food resource of adult Heligmosomoides polygyrus in the small intestine. J. Parasitol. 80, 24–28 (1994).CAS 
PubMed 
Article 

Google Scholar 
Starr, L. M., Scott, M. E. & Koski, K. G. Protein deficiency and intestinal nematode infection in pregnant mice differentially impact fetal growth through specific stress hormones, growth factors, and cytokines. J. Nutr. 145, 41–50 (2015).CAS 
PubMed 
Article 

Google Scholar 
Herring, C. M., Bazer, F. W., Johnson, G. A. & Wu, G. Impacts of maternal dietary protein intake on fetal survival, growth, and development. Exp. Biol. Med. (Maywood). 243, 525–533 (2018).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Starr, L. M., Odiere, M. R., Koski, K. G. & Scott, M. E. Protein deficiency alters impact of intestinal nematode infection on intestinal, visceral and lymphoid organ histopathology in lactating mice. Parasitology 141, 801–813 (2014).CAS 
PubMed 
Article 

Google Scholar 
Bastian, T. W., von Hohenberg, W. C., Mickelson, D. J., Lanier, L. M. & Georgieff, M. K. Iron deficiency impairs developing hippocampal neuron gene expression, energy metabolism, and dendrite complexity. Dev. Neurosci. 38, 264–276 (2016).CAS 
PubMed 
Article 

Google Scholar 
Bastian, T. W., Rao, R., Tran, P. V. & Georgieff, M. K. The effects of early-life iron deficiency on brain energy metabolism. Neurosci. Insights. 15, 2633105520935104. https://doi.org/10.1177/2633105520935104 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Gould, J. M. et al. Mouse maternal protein restriction during preimplantation alone permanently alters brain neuron proportion and adult short-term memory. Proc. Natl. Acad. Sci. 115, E7398–E7407. https://doi.org/10.1073/pnas.1721876115 (2018).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Radlowski, E. & Johnson, R. Perinatal iron deficiency and neurocognitive development. Front. Hum. Neurosci. 7, 585 (2013).PubMed 
PubMed Central 
Article 

Google Scholar 
Rytych, J. L. et al. Early life iron deficiency impairs spatial cognition in neonatal piglets. J. Nutr. 142, 2050–2056 (2012).CAS 
PubMed 
Article 

Google Scholar 
Snyder, J. S., Hong, N. S., McDonald, R. J. & Wojtowicz, J. M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843–852 (2005).CAS 
PubMed 
Article 

Google Scholar 
Brązert, M. et al. Expression of genes involved in neurogenesis, and neuronal precursor cell proliferation and development: Novel pathways of human ovarian granulosa cell differentiation and transdifferentiation capability in vitro. Mol. Med. Rep. 21, 1749–1760 (2020).PubMed 
PubMed Central 

Google Scholar 
van Praag, H., Christie, B. R., Sejnowski, T. J. & Gage, F. H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 13427–13431 (1999).ADS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Li, H. et al. Regular treadmill running improves spatial learning and memory performance in young mice through increased hippocampal neurogenesis and decreased stress. Brain. Res. 1531, 1–8 (2013).MathSciNet 
CAS 
PubMed 
Article 

Google Scholar 
Odiere, M. R., Scott, M. E., Leroux, L. P., Dzierszinski, F. S. & Koski, K. G. Maternal protein deficiency during a gastrointestinal nematode infection alters developmental profile of lymphocyte populations and selected cytokines in neonatal mice. J. Nutr. 143, 100–107 (2013).CAS 
PubMed 
Article 

Google Scholar 
El Ahdab, N., Haque, M., Madogwe, E., Koski, K. G. & Scott, M. E. Maternal nematode infection upregulates expression of Th2/Treg and diapedesis related genes in the neonatal brain. Sci. Rep. 11, 22082. https://doi.org/10.1038/s41598-021-01510-0 (2021).ADS 
CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Hein, A. M. et al. Sustained hippocampal IL-1β overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav. Immun. 24, 243–253 (2010).CAS 
PubMed 
Article 

Google Scholar 
Derecki, N. C. et al. Regulation of learning and memory by meningeal immunity: A key role for IL-4. Exp. Med. 207, 1067–1080 (2010).CAS 
Article 

Google Scholar 
Brombacher, T. M. et al. IL-4R alpha deficiency influences hippocampal-BDNF signaling pathway to impair reference memory. Sci. Rep. 10, 16506. https://doi.org/10.1038/s41598-020-73574-3 (2020).CAS 
Article 
PubMed 
PubMed Central 

Google Scholar 
Mizuno, M., Yamada, K., Olariu, A., Nawa, H. & Nabeshima, T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 20, 7116–7121 (2000).CAS 
PubMed 
PubMed Central 
Article 

Google Scholar 
Miranda, M., Morici, J. F., Zanoni, M. B. & Bekinschtein, P. Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Front. Cell. Neurosci. 13. https://doi.org/10.3389/fncel.2019.00363 (2019).Williamson, L. L. et al. Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection. Brain Behav. Immun. 51, 14–28 (2016).CAS 
PubMed 
Article 

Google Scholar 
McKay, D. M. The immune response to and immunomodulation by Hymenolepis diminuta. Parasitology 137, 385–394 (2010).CAS 
PubMed 
Article 

Google Scholar 
Meyer, U., Feldon, J. & Fatemi, S. H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33, 1061–1079 (2009).CAS 
PubMed 
Article 

Google Scholar 
Johnston, C. J. C. et al. Cultivation of Heligmosomoides polygyrus: an immunomodulatory nematode parasite and its secreted products. J. Vis. Exp. e52412–e52412. https://doi.org/10.3791/52412 (2015).Valanparambil, R. M. et al. Production and analysis of immunomodulatory excretory-secretory products from the mouse gastrointestinal nematode Heligmosomoides polygyrus bakeri. Nat. Protoc. 9, 2740–2754 (2014).CAS 
PubMed 
Article 

Google Scholar 
Murai, T., Okuda, S., Tanaka, T. & Ohta, H. Characteristics of object location memory in mice: Behavioral and pharmacological studies. Physiol. Behav. 90, 116–124 (2007).CAS 
PubMed 
Article 

Google Scholar 
Patil, S. S., Sunyer, B., Hoger, H. & Lubec, G. Evaluation of spatial memory of C57BL/6J and CD1 mice in the Barnes maze, the Multiple T-maze and in the Morris water maze. Behav. Brain. Res. 198, 58–68 (2009).PubMed 
Article 

Google Scholar 
R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2020).Wickham, H. ggplot2: Elegant graphics for data analysis (Springer-Verlag, 2016).MATH 
Book 

Google Scholar 
Lazic, S. E. The problem of pseudoreplication in neuroscientific studies: Is it affecting your analysis?. BMC Neurosci. 11, 5. https://doi.org/10.1186/1471-2202-11-5 (2010).Article 
PubMed 
PubMed Central 

Google Scholar 
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. & Smith, G. M. Mixed effects models and extensions in ecology with R. Vol. 1–574 (2009).Bates, D., Maechler, M., Bolker, B. & Steve, W. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

Google Scholar 
Fox, J. & Sanford, W. An R Companion to Applied Regression. 3 edn, (Sage, 2019).emmeans: Estimated marginal means, aka least-squares means v. 1.4.8 (R package, 2020).RVAideMemoire: Testing and plotting procedures for biostatistics. v. 0.9-78 (R package, 2020).DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models v. 0.3.3.0 (R package, 2020).Delignette-Muller, M. L. & Dutang, C. fitdistrplus: An R package for fitting distributions. J. Stat. Softw. 64, 1–34 (2015).Article 

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This study reveals that various measures of bee diversity-including abundance, richness, and assemblage patterns are influenced by vane color and light reflectance patterns when passively sampling bees with vane traps. In particular, brightly colored vanes with higher light reflectance within 400–600 nm range attracted a greater diversity of bees in traps placed in a livestock pasture ecosystem. Effectiveness of blue and yellow vane traps had been compared previously in different ecosystems, for instance in apple orchards17, both woodland and open agriculture farmland13, and adjacent to Helianthus spp. (Asteraceae) field27. In all these studies, blue vane trap captured more bee species and 5–6 times more individuals compared to yellow vane trap.In the current study, we assessed a different design and size of vanes and a wider array of vane colors and reflectance patterns attached to sample collection jars. In particular, we used bright blue and yellow vanes that were made of plastic sheets covered with a micro-prismatic retro-reflective sheeting that provides better daytime and nighttime brightness as well as high visibility and durability. These vanes showed higher light reflectance and captured the most bees and bee species in this study (Table 2). Similar material was used on red vanes as well, but the light reflectance from those vanes was relatively lower, and as a result captured fewer bees. Traps with bright blue vanes performed especially well in terms of rates of bee capture (Fig. 2; 11.1 bees per trap per sampling date) and rates of species accumulation (Fig. 3). Bright yellow traps exhibited the second highest values for capture rates (Fig. 2; 6.6 bees per trap per sampling date) and species accumulation (Fig. 3), but these rates were not deemed significantly different from some other colors in which the reflective sheeting was not used, such as dark yellow, dark blue and purple.Bees use visual clues for detection, recognition, and memorization of floral resources in the foraging landscape7,28. The intensity of light reflected from different colors of vanes in traps affect number of bees attracted toward the trap10. Most bees can recognize colors that fall between 300 to 600 nm visual spectrums29. While the information related to the vision of many solitary and wild bees is not available, in the case of honey bees (Apis mellifera), color vision is trichromatic with highly sensitive photoreceptors at 344 nm (ultraviolet), 436 nm (blue) and 544 nm (green)30.In this study, colored vanes at a higher light reflectance between 400 to 600 nm attracted the highest number bee species in these passive traps. Capture rate differed among traps with different colored vanes in the current study, which can be explained by sensitivity of visual spectrum of bees and variation in the light reflectance of vanes of these traps. For example, bright blue vanes had two peaks of higher light reflectance, initially in 450–455 nm range and second peak with  > 800 nm. Such higher reflectance peak within the optimal range of bee vision may have played an important role in attracting abundant and diverse bee species to these passive traps. Similarly, bright yellow captured second largest number of bees, also had higher light reflectance peak within 600 nm but gradually decreased with increasing wavelength. Though bees have color spectrum from UV to orange31, they are sensitive to color spectrum between blue, green and ultraviolet32, which is a type of trichromatic vision system28. In one study33, red color vanes showed relatively lower light reflectance within 600 nm range, but had higher reflectance later in the spectrum, and this could be a reason why a low number of bees were collected in the traps. Past research showed contradictory views regarding the ability of bees to perceive red color. For instance, an early researcher in this field33, reported that bees recognize red color objects; however, other researchers had reported inability of bees to perceive34 or discriminate red from other colors35,36. It was argued that the bees see up to 650 nm in the visual spectrum and may not miss red colored flowers while foraging. However, other factors such as background (vegetation) color could also be contributing to bees’ ability to navigate different vane or flower colors in a livestock pasture landscape. Generally bees use color contrast to locate flower source, and hence neutral colors such as white are usually ignored29. Ultraviolet signal can make flowers more or less attractive to bees depending on whether it increases or decreases color contrast37. For example, UV color component in yellow38 and red39 flower increases chromatic contrast of these colored flowers with their background contributing attractiveness to the flowers. However, UV-reflecting white flowers decreases attractiveness for bees40.Different species of bees responded to different colors of vane traps. Out of the 49 bee species collected in this study, only nine bee species were found in all vane color types, whereas 14 species were found in only one trap color. For instance, out of five bumble bee species, two were found in all six vane colors, one was found in five colors, and two species (Bombus bimaculatus and B. fervidus) were only found in the traps with bright blue vanes. Many of the species that were only found in one trap color- Calliopsis andreniformis (1, bright yellow), Ceratina dupla (1, bright yellow), Diadasia afflicta (1, bright blue), Diadasia enavata (1, dark blue), Halictus rubicundus (1, dark yellow), Hylaeus mesillae (1, red), Lasioglossum tegulare (1, bright blue), Lasioglossum trigeminum (1, purple), Megachile montivaga (1, dark yellow), Melitoma taurea (1, bright blue), Svastra atripes (1, bright blue), and Triepeolus lunatus (1, dark yellow) were singletons and it was impossible to know if this represented a true preference or pattern. Our analysis of assemblage patterns after aggregating bees at the genus level, did show a gradient-like response in bee-color associations (Fig. 4), ranging from dark blue to yellows (with no strong associations found with red vanes). These patterns may be used to guide future (passive trap-based) sampling efforts to monitor bee diversity or to target specific bee species in livestock pastures or other ecosystems. While the bright blue and yellow traps with reflective sheeting were particularly attractive to bees, dark blue and purple traps also had relatively high levels of abundance and richness and collected higher number of Melissodes. Purple, as a color, is less commonly used than blue and yellow traps in bee monitoring. While this study shows that purple may be a viable option for bee collection, it’s similar assemblage pattern (Fig. 4) and low level of complementarity with dark blue traps (Table 2) suggests that it may be redundant with blue traps that are already commonly used. Differences in species- and sex-specific associations of bees with different colors of sampling traps had also been reported in previous studies41.Most of the bees collected in the current study were from Halictidae family (77.6%) followed by Apidae. However, few bee species in the families Andrenidae, Colletidae, and Megachilidae were collected. Consistent with our findings, others42 reported that bees of the Halictidae family were the most abundant bees in rangeland of Texas. The most common species found in this study were Au. aurata, L. disparile, L. imitatum, and Ag. texanus). In our previous studies we have found similar bee diversity in this study region18. Pollinator species richness and diversity as well as population distribution in livestock pasture vary during the season43. Mid-July to mid-August is the latter half of the summer season in the Southeastern USA, and the sampling period may have missed bee species that emerge earlier in the season and are reported in other studies42,43.Overall, the findings of this study showed that the wild bees responded differently to passive traps with colored vanes of different light wavelength and reflectivity when deployed in a livestock pasture ecosystem. Among six different colors of vanes (dark blue, bright blue, dark yellow, bright yellow, purple and red), the bright blue traps captured the highest number of individuals and species of bees. This could be due to an appropriate match between the visual spectrum of bees and the light reflectance spectrum of vanes, which were made of a micro-prismatic retro-reflective material. Bees responded similarly to traps with other colors of vanes, except for red vane traps, which captured the lowest number of bees. The findings of this study would be useful in understanding bee vision and responses to passive traps, and, such information would help in optimizing bee sampling methods for future monitoring efforts. More