More stories

  • in

    Morphological response accompanying size reduction of belemnites during an Early Jurassic hyperthermal event modulated by life history

    1.Reddin, C. J., Kocsis, Á. T., Aberhan, M. & Kiessling, W. Victims of ancient hyperthermal events herald the fates of marine clades and traits under global warming. Glob. Chang. Biol. 27, 868–878 (2021).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    2.Reddin, C. J., Kocsis, Á. T. & Kiessling, W. Marine invertebrate migrations trace climate change over 450 million years. Glob. Ecol. Biogeogr. 27, 704–713 (2018).Article 

    Google Scholar 
    3.Kordas, R. L., Harley, C. D. G. & O’Connor, M. I. Community ecology in a warming world: The influence of temperature on interspecific interactions in marine systems. J. Exp. Mar. Bio. Ecol. 400, 218–226 (2011).Article 

    Google Scholar 
    4.Poloczanska, E. S. et al. Responses of marine organisms to climate change across oceans. Front. Mar. Sci. 3, 1–21 (2016).Article 

    Google Scholar 
    5.Hanken, J. & Wake, D. B. Miniaturization of body size: Organismal consequences and evolutionary significance. Annu. Rev. Ecol. Syst. 24, 501–519 (1993).Article 

    Google Scholar 
    6.Sheridan, J. A. & Bickford, D. Shrinking body size as an ecological response to climate change. Nat. Clim. Chang. 1, 401–406 (2011).ADS 
    Article 

    Google Scholar 
    7.Forster, J., Hirst, A. G. & Atkinson, D. Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc. Natl. Acad. Sci. U. S. A. 109, 19310–19314 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Ohlberger, J. Climate warming and ectotherm body size – from individual physiology to community ecology. Funct. Ecol. 27, 991–1001 (2013).Article 

    Google Scholar 
    9.Garilli, V. et al. Physiological advantages of dwarfing in surviving extinctions in high-CO 2 oceans. Nat. Clim. Chang. 5, 678–682 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    10.Daufresne, M., Lengfellner, K. & Sommer, U. Global warming benefits the small in aquatic ecosystems. Proc. Natl. Acad. Sci. U. S. A. https://doi.org/10.1073/pnas.0902080106 (2009).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Verberk, W. C. E. P. et al. Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen. Biol. Rev. 96, 247–268 (2021).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    12.Angilletta, M. J., Steury, T. D. & Sears, M. W. Temperature, growth rate, and body size in ectotherms: Fitting pieces of a life-history puzzle. Integr. Comp. Biol. 44, 498–509 (2004).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    13.Hoving, H. J. T. et al. Extreme plasticity in life-history strategy allows a migratory predator (jumbo squid) to cope with a changing climate. Glob. Chang. Biol. 19, 2089–2103 (2013).ADS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Angilletta, M. J. & Dunham, A. E. The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am. Nat. 162, 332–342 (2003).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.Vinarski, M. V. On the applicability of Bergmann’s rule to ectotherms: the state of the art. Biol. Bull. Rev. 4, 232–242 (2014).Article 

    Google Scholar 
    16.Atkinson, D. Temperature and organism size: a biological law for organisms?. Adv. Ecol. Res. 25, 1–58 (1994).Article 

    Google Scholar 
    17.Atkinson, D. Effects of temperature on the size of aquatic ectotherms: Exceptions to the general rule. J. Therm. Biol. 20, 61–74 (1995).Article 

    Google Scholar 
    18.Forster, J. & Hirst, A. G. The temperature-size rule emerges from ontogenetic differences between growth and development rates. Funct. Ecol. 26, 483–492 (2012).Article 

    Google Scholar 
    19.Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. & Charnov, E. L. Effects of size and temperature on metabolic rate. Science 293, 2248–2251 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    20.Schulte, P. M. The effects of temperature on aerobic metabolism: Towards a mechanistic understanding of the responses of ectotherms to a changing environment. J. Exp. Biol. 218, 1856–1866 (2015).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73 (2002).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Riemer, K., Anderson-Teixeira, K. J., Smith, F. A., Harris, D. J. & Ernest, S. K. M. Body size shifts influence effects of increasing temperatures on ectotherm metabolism. Glob. Ecol. Biogeogr. 27, 958–967 (2018).Article 

    Google Scholar 
    23.Rosa, R. et al. Ocean warming enhances malformations, premature hatching, metabolic suppression and oxidative stress in the early life stages of a keystone squid. PLoS ONE 7, e38282 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Pecl, G. T. & Jackson, G. D. The potential impacts of climate change on inshore squid: Biology, ecology and fisheries. Rev. Fish Biol. Fish. 18, 373–385 (2008).Article 

    Google Scholar 
    25.Twitchett, R. J. The Lilliput effect in the aftermath of the end-Permian extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol. 252, 132–144 (2007).Article 

    Google Scholar 
    26.Harries, P. J. & Knorr, P. O. What does the ‘Lilliput Effect’ mean?. Palaeogeogr. Palaeoclimatol. Palaeoecol. 284, 4–10 (2009).Article 

    Google Scholar 
    27.Metcalfe, B., Twitchett, R. J. & Price-Lloyd, N. Changes in size and growth rate of ‘Lilliput’ animals in the earliest Triassic. Palaeogeogr. Palaeoclimatol. Palaeoecol. 308, 171–180 (2011).Article 

    Google Scholar 
    28.Chu, D. et al. Lilliput effect in freshwater ostracods during the Permian-Triassic extinction. Palaeogeogr. Palaeoclimatol. Palaeoecol. 435, 38–52 (2015).Article 

    Google Scholar 
    29.Urbanek, A. Biotic crises in the history of upper silurian graptoloids: a palaeobiological model. Hist. Biol. https://doi.org/10.1080/10292389309380442 (1993).Article 

    Google Scholar 
    30.Urlichs, M. Stunting in invertebrates from the type area of the Cassian Formation (Early Carnian) of the dolomites (Italy). GeoAlp 8, 164–169 (2011).
    Google Scholar 
    31.Morten, S. D. & Twitchett, R. J. Fluctuations in the body size of marine invertebrates through the Pliensbachian-Toarcian extinction event. Palaeogeogr. Palaeoclimatol. Palaeoecol. https://doi.org/10.1016/j.palaeo.2009.08.023 (2009).Article 

    Google Scholar 
    32.Piazza, V., Ullmann, C. V. & Aberhan, M. Temperature-related body size change of marine benthic macroinvertebrates across the Early Toarcian Anoxic Event. Sci. Rep. 10, 1–13 (2020).Article 
    CAS 

    Google Scholar 
    33.Calosi, P., Putnam, H. M., Twitchett, R. J. & Vermandele, F. Marine metazoan modern mass extinction: improving predictions by integrating fossil, modern, and physiological data. Ann. Rev. Mar. Sci. 11, 369–390 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    34.Gerber, S. Comparing the differential filling of morphospace and allometric space through time: the morphological and developmental dynamics of Early Jurassic ammonoids. Paleobiology 37, 369–382 (2011).Article 

    Google Scholar 
    35.Pálfy, J. & Smith, P. L. Synchrony between Early Jurassic extinction, oceanic anoxic event, and the Karoo-Ferrar flood basalt volcanism. Geology 28, 747–750 (2000).ADS 
    Article 

    Google Scholar 
    36.Caruthers, A. H., Smith, P. L. & Gröcke, D. R. The Pliensbachian-Toarcian (Early Jurassic) extinction, a global multi-phased event. Palaeogeogr. Palaeoclimatol. Palaeoecol. 386, 104–118 (2013).Article 

    Google Scholar 
    37.Wignall, P. B. Large igneous provinces and mass extinctions. Earth Sci. Rev. 53, 1–33 (2001).ADS 
    CAS 
    Article 

    Google Scholar 
    38.Percival, L. M. E. et al. Globally enhanced mercury deposition during the end-Pliensbachian extinction and Toarcian OAE: A link to the Karoo-Ferrar Large Igneous Province. Earth Planet. Sci. Lett. 428, 267–280 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    39.Foster, G. L., Hull, P., Lunt, D. J. & Zachos, J. C. Placing our current ‘hyperthermal’ in the context of rapid climate change in our geological past. Phil. Trans. R. Soc. A 376, 20170086 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    40.Suan, G. et al. Secular environmental precursors to Early Toarcian (Jurassic) extreme climate changes. Earth Planet. Sci. Lett. 290, 448–458 (2010).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Fantasia, A. et al. Global versus local processes during the Pliensbachian-Toarcian transition at the Peniche GSSP, Portugal: A multi-proxy record. Earth Sci. Rev. 198, 102932 (2019).CAS 
    Article 

    Google Scholar 
    42.Müller, T. et al. Ocean acidification during the early Toarcian extinction event: Evidence from Boron isotopes in brachiopods. Geology 48, 1184–1188 (2020).ADS 
    Article 

    Google Scholar 
    43.Suan, G., Mattioli, E., Pittet, B., Mailliot, S. & Lécuyer, C. Evidence for major environmental perturbation prior to and during the Toarcian (Early Jurassic) oceanic anoxic event from the Lusitanian Basin Portugal. Paleoceanography 23, A1202 (2008).ADS 
    Article 

    Google Scholar 
    44.Dera, G. et al. High-resolution dynamics of early Jurassic marine extinctions: The case of Pliensbachian-Toarcian ammonites (Cephalopoda). J. Geol. Soc. London 167, 21–33 (2010).CAS 
    Article 

    Google Scholar 
    45.Dera, G. et al. Climatic ups and downs in a disturbed Jurassic world. Geology 39, 215–218 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    46.Miguez-Salas, O., Rodríguez-Tovar, F. J. & Duarte, L. V. Selective incidence of the Toarcian oceanic anoxic event on macroinvertebrate marine communities: a case from the Lusitanian basin Portugal. Lethaia 50, 548–560 (2017).Article 

    Google Scholar 
    47.Correia, V. F., Riding, J. B., Duarte, L. V., Fernandes, P. & Pereira, Z. The palynological response to the Toarcian Oceanic Anoxic Event (Early Jurassic) at Peniche, Lusitanian Basin, western Portugal. Mar. Micropaleontol. 137, 46–63. https://doi.org/10.1016/j.marmicro.2017.10.004 (2017).ADS 
    Article 

    Google Scholar 
    48.Rita, P., Nätscher, P., Duarte, L. V., Weis, R. & De Baets, K. Mechanisms and drivers of belemnite body-size dynamics across the Pliensbachian-Toarcian crisis. R. Soc. Open Sci. 6, 190494 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Caswell, B. A. & Coe, A. L. The impact of anoxia on pelagic macrofauna during the Toarcian Oceanic Anoxic Event (Early Jurassic). Proc. Geol. Assoc. 125(4), 383–391. https://doi.org/10.1016/j.pgeola.2014.06.001 (2014).Article 

    Google Scholar 
    50.Ullmann, C. V., Thibault, N., Ruhl, M., Hesselbo, S. P. & Korte, C. Effect of a Jurassic oceanic anoxic event on belemnite ecology and evolution. Proc. Natl. Acad. Sci. U. S. A. 111, 10073–10076 (2014).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Dera, G., Toumoulin, A. & de Baets, K. Diversity and morphological evolution of Jurassic belemnites from South Germany. Palaeogeogr. Palaeoclimatol. Palaeoecol. 457, 80–97 (2016).Article 

    Google Scholar 
    52.Neige, P., Weis, R. & Fara, E. Ups and downs of belemnite diversity in the Early Jurassic of Western Tethys. Palaeontology 64, 263–283 (2021).Article 

    Google Scholar 
    53.Rita, P., De Baets, K. & Schlott, M. Rostrum size differences between Toarcian belemnite battlefields. Foss. Rec. 21, 171–182 (2018).Article 

    Google Scholar 
    54.Rita, P. et al. Biogeographic patterns of belemnite body size responses to episodes of environmental crisis. PeerJ Prepr. (2019).55.Hoffmann, R. & Stevens, K. The palaeobiology of belemnites – foundation for the interpretation of rostrum geochemistry. Biol. Rev. 95, 94–123 (2020).Article 

    Google Scholar 
    56.Adams, D. C. & Otárola-Castillo, E. Geomorph: An r package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).Article 

    Google Scholar 
    57.Schlegelmilch, R. Die Belemniten des süddeutschen Jura. Die Belemniten des süddeutschen Jura https://doi.org/10.1007/978-3-8274-3083-0 (1998).Article 

    Google Scholar 
    58.McArthur, J. M. et al. Sr-isotope stratigraphy (87Sr/86Sr) of the lowermost Toarcian of Peniche, Portugal, and its relation to ammonite zonations. Newsletters Stratigr. 53, 297–312 (2020).Article 

    Google Scholar 
    59.Hesselbo, S. P., Jenkyns, H. C., Duarte, L. V. & Oliveira, L. C. V. Carbon-isotope record of the Early Jurassic (Toarcian) Oceanic Anoxic Event from fossil wood and marine carbonate (Lusitanian Basin, Portugal). Earth Planet. Sci. Lett. 253, 455–470 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    60.Klug, C., Schweigert, G., Fuchs, D., Kruta, I. & Tischlinger, H. Adaptations to squid-style high-speed swimming in Jurassic belemnitids. Biol. Lett. 12, 20150877 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Seibel, B. A., Thuesen, E. V., Childress, J. J. & Gorodezky, L. A. Decline in pelagic cephalopod metabolism with habitat depth reflects differences in locomotory efficiency. Biol. Bull. 192, 262–278 (1997).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    62.Mattioli, E., Pittet, B., Petitpierre, L. & Mailliot, S. Dramatic decrease of pelagic carbonate production by nannoplankton across the Early Toarcian anoxic event (T-OAE). Glob. Planet. Change 65, 134–145 (2009).ADS 
    Article 

    Google Scholar 
    63.Chamberlain, J. A. Locomotion in ancient seas: Constraint and opportunity in Cephalopod adaptive design. Geobios 15, 49–61 (1993).Article 

    Google Scholar 
    64.Rexfort, A. & Mutterlose, J. The role of biogeography and ecology on the isotope signature of cuttlefishes (Cephalopoda, Sepiidae) and the impact on belemnite studies. Palaeogeogr. Palaeoclimatol. Palaeoecol. 284, 153–163 (2009).Article 

    Google Scholar 
    65.Holland, S. M. The quality of the fossil record: a sequence stratigraphic perspective. Paleobiology 26, 148–168 (2000).Article 

    Google Scholar 
    66.Holland, S. M. The non-uniformity of fossil preservation. Philos. Trans. R. Soc. B Biol. Sci. 371, 2 (2016).
    Google Scholar 
    67.Korn, D. Impact of enviornmental perturbations o heterochronic develpments in Palaeozoic ammonoids. Evol. Chang. Heterochrony 245–260 (1995).68.Yacobucci, M. M. Plasticity of developmental timing as the underlying cause of high speciation rates in ammonoids. in Advancing research on living and fossil cephalopods 59–76 (Springer, Boston, MA, 1999).69.Landman, N. H. & Gyssant, J. R. Heterochrony and ecology in Jurassic and Cretaceous ammonites. Geobios 26, 247–255 (1993).Article 

    Google Scholar 
    70.McNamara, K. J. Heterochrony: the evolution of development. Evol. Educ. Outreach 5, 203–218 (2012).Article 

    Google Scholar 
    71.Dahlke, F. T., Wohlrab, S., Butzin, M. & Pörtner, H. O. Thermal bottlenecks in the life cycle define climate vulnerability of fish. Science 369, 65–70 (2020).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    72.Pörtner, H. O. & Farrell, A. P. Ecology: Physiology and climate change. Science https://doi.org/10.1126/science.1163156 (2008).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    73.Pimentel, M. S. et al. Impact of ocean warming on the early ontogeny of cephalopods: A metabolic approach. Mar. Biol. 159, 2051–2059 (2012).Article 

    Google Scholar 
    74.Komoroske, L. M. et al. Ontogeny influences sensitivity to climate change stressors in an endangered fish. Conserv. Physiol. 2, 1–13 (2014).Article 
    CAS 

    Google Scholar 
    75.Pörtner, H. O., Bock, C. & Mark, F. C. Oxygen- & capacity-limited thermal tolerance: Bridging ecology & physiology. J. Exp. Biol. 220, 2685–2696 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Harnik, P. G., Simpson, C. & Payne, J. L. Long-term differences in extinction risk among the seven forms of rarity. Proc. R. Soc. B Biol. Sci. 279, 4969–4976 (2012).Article 

    Google Scholar 
    77.Reddin, C. J., Kocsis, Á. T. & Kiessling, W. Climate change and the latitudinal selectivity of ancient marine extinctions. Paleobiology 45, 70–84 (2019).Article 

    Google Scholar 
    78.Dorey, N. et al. Ocean acidification and temperature rise: Effects on calcification during early development of the cuttlefish Sepia officinalis. Mar. Biol. 160, 2007–2022 (2013).CAS 
    Article 

    Google Scholar 
    79.Sigwart, J. D. et al. Elevated pCO2 drives lower growth and yet increased calcification in the early life history of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) Julia. ICES J. Mar. Sci. 73, 970–980 (2016).Article 

    Google Scholar 
    80.Gutowska, M. A., Melzner, F., Pörtner, H. O. & Meier, S. Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis. Mar. Biol. 157, 1653–1663 (2010).CAS 
    Article 

    Google Scholar 
    81.Kaplan, M. B., Mooney, T. A., McCorkle, D. C. & Cohen, A. L. Adverse effects of ocean acidification on early development of squid (Doryteuthis pealeii). PLoS ONE 8, e63714 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Otjacques, E. et al. Cuttlefish buoyancy in response to food availability and ocean acidification. Biology (Basel). https://doi.org/10.3390/biology9070147 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    83.Neige, P. & Boletzky, S. Morphometrics of the shell of three Sepia species (Mollusca: Cephalopoda): Intra- and interspecific variation. Zool. Beitraege. 38, 137–156 (1997).
    Google Scholar 
    84.Rita, P., Weis, R., Duarte, L. V. & De Baets, K. Taxonomical diversity and palaeobiogeographical affinity of belemnites from the Pliensbachian-Toarcian GSSP (Lusitanian Basin, Portugal). Pap. Palaeontol. https://doi.org/10.1002/spp2.1343 (2020).Article 

    Google Scholar 
    85.MacArthur, R. H. Geographical ecology: patterns in the distribution of species. (Princeton University Press, 1972).86.Gaston, K. J. The structure and dynamics of geographic ranges. (Oxford University Press on Demand, 2003).87.Duarte, L. Sequence stratigraphy and depositional setting of the Pliensbachian and Toarcian marly limestones in the Lusitanian Basin Portugal. Ciências da Terra 16, 17–23 (2007).
    Google Scholar 
    88.Reddin, C. J., Nätscher, P. S., Kocsis, Á. T., Pörtner, H.-O. & Kiessling, W. Marine clade sensitivities to climate change conform across timescales. Nat. Clim. Chang. 10, 249–253 (2020).ADS 
    Article 

    Google Scholar 
    89.Doyle, P. & Kelly, R. A. The Jurassic and Cretaceous belemnites of Kong Karls Land, Svalbard. (Norsk Polarinstitutt Oslo, 1988).90.Doyle, P. New records of dimitobelid belemnites from the cretaceous of james ross island Antarctica. Alcheringa 14, 159–175 (1990).Article 

    Google Scholar 
    91.Fedorov, A. et al. 3D Slicer as an image computing platform for the Quantitative Imaging Network. Magn. Reson. Imaging https://doi.org/10.1016/j.mri.2012.05.001 (2012).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    92.Rohatgi, A., Rehberg, S. & Stanojevic, Z. Webplotdigitizer: Version 4.1 of Webplotdigitizer. (2018).https://doi.org/10.5281/zenodo.1137880.93.Plate, T. & Heiberger, R. Package ‘ abind ’. (2016).94.Collyer, M. L. & Adams, D. C. RRPP: An r package for fitting linear models to high-dimensional data using residual randomization. Methods Ecol. Evol. 9, 1772–1779 (2018).Article 

    Google Scholar 
    95.Sherratt, E. Quick Guide to Geomorph v. 2.0. public.iastate.edu (2014).96.Torchiano, M. Package ‘ effsize ’. (2020).97.Gotelli, N. J., Dorazio, R. M., Ellison, A. M. & Grossman, G. D. Detecting temporal trends in species assemblages with bootstrapping procedures and hierarchical models. Philos. Trans. 365, 3621–3631 (2010).Article 

    Google Scholar 
    98.Hervé, M. Package ‘ RVAideMemoire ’. (2021).99.Mangiafico, S. Package ‘ rcompanion ’. (2021).100.Oksanen, J. et al. Package ‘vegan’ title community ecology package. Commun. Ecol. Packag. 2, 1–297 (2019).MathSciNet 

    Google Scholar 
    101.Pinheiro, J. et al. Package ‘nlme’. (2021).102.Dormann, C. F. et al. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography (Cop.) 36, 27–46 (2013).Article 

    Google Scholar 
    103.R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria (2019).104.Garnier, S., Ross, N., Rudis, B. & Sciaini, M. Package ‘viridis’. (2021). More

  • in

    Author Correction: Determinants of genetic variation across eco-evolutionary scales in pinnipeds

    These authors contributed equally: Claire R. Peart, Sergio Tusso, Saurabh D. Pophaly.Science of Life Laboratories and Department of Evolutionary Biology, Uppsala University, Uppsala, SwedenClaire R. Peart, Sergio Tusso, Chi-Chih Wu, Aaron B. A. Shafer & Jochen B. W. WolfDivision of Evolutionary Biology, Faculty of Biology, LMU Munich, Planegg-Martinsried, GermanyClaire R. Peart, Sergio Tusso, Saurabh D. Pophaly, Fidel Botero-Castro & Jochen B. W. WolfMax Planck Institute for Plant Breeding Research, Cologne, GermanySaurabh D. PophalyLaboratorio de Ecología de Pinnípedos ‘Burney J. Le Boeuf’, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Baja California Sur, MéxicoDavid Aurioles-GamboaDepartment of Natural Sciences, University of Houston-Downtown, Houston, TX, USAAmy B. BairdDepartment of Ecology and Conservation Biology, Texas A&M University, College Station, TX, USAJohn W. BickhamBritish Antarctic Survey, Natural Environment Research Council, Cambridge, UKJaume Forcada & Joseph I. HoffmanElephant Seal Research Group, Sea Lion Island, Falkland IslandsFilippo Galimberti & Simona SanvitoDepartment of Anatomy, University of Otago, Dunedin, New ZealandNeil J. GemmellDepartment of Animal Behaviour, Bielefeld University, Bielefeld, GermanyJoseph I. HoffmanNorwegian Polar Institute, Fram Centre, Tromsø, NorwayKit M. Kovacs & Christian LydersenDepartment of Environmental and Biological Sciences, University of Eastern Finland, Joensuu, FinlandMervi Kunnasranta & Tommi NymanNatural Resources Institute Finland (Luke), Joensuu, FinlandMervi KunnasrantaDepartment of Ecosystems in the Barents Region, Norwegian Institute of Bioeconomy Research, Svanhovd Research Station, Svanvik, NorwayTommi NymanLaboratory of Mammal Ecology, Universidade do Vale do Rio dos Sinos, São Leopoldo, BrazilLarissa Rosa de OliveiraNational Oceanic and Atmospheric Administration, National Marine Fisheries Service, Alaska Fisheries Science Center, Marine Mammal Laboratory, Seattle, WA, USAAnthony J. OrrThe Saimaa Ringed Seal Genome Project, Institute of Biotechnology, University of Helsinki, Helsinki, FinlandMia ValtonenForensic Science & Environmental Life Sciences, Trent University, Peterborough, Ontario, CanadaAaron B. A. Shafer More

  • in

    Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants

    1.Valles, S. M. et al. A picorna-like virus from the red imported fire ant, Solenopsis invicta: Initial discovery, genome sequence, and characterization. Virology 328(1), 151–157. https://doi.org/10.1016/j.virol.2004.07.016 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    2.Russell, J. A. The ants (Hymenoptera: Formicidae) are unique and enigmatic hosts of prevalent Wolbachia (Alphaproteobacteria) symbionts. Myrmecol. News 16, 7–23 (2012).
    Google Scholar 
    3.Mongkolsamrit, S. et al. Life cycle, host range and temporal variation of Ophiocordyceps unilateralis/Hirsutella formicarum on Formicine ants. J. Invertebr. Pathol. 111(3), 217–224. https://doi.org/10.1016/j.jip.2012.08.007 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    4.Espadaler, X. & Santamaria, S. Ecto-and endoparasitic fungi on ants from the Holarctic region. Psyche https://doi.org/10.1155/2012/168478 (2012).Article 

    Google Scholar 
    5.Boomsma, J. J., Schmid-Hempel, P. & Hughes, W. O. H. Life histories and parasite pressure across the major groups of social insects. in Insect Evolutionary Ecology: Proceedings of the Royal Entomological Society’s 22nd Symposium, Reading, UK, 2003. (CABI Publishing, 2005).6.Lachaud, J. P., Lenoir, A. & Hughes, D. P. Ants and their parasites. Psyche https://doi.org/10.1155/2013/264279 (2013).Article 

    Google Scholar 
    7.de Bekker, C., Will, I., Das, B. & Adams, R. M. The ants (Hymenoptera: Formicidae) and their parasites: Effects of parasitic manipulations and host responses on ant behavioral ecology. Myrmecol. News 28, 1–24. https://doi.org/10.25849/myrmecol.news_028:001 (2018).Article 

    Google Scholar 
    8.Witek, M., Barbero, F. & Markó, B. Myrmica ants host highly diverse parasitic communities: From social parasites to microbes. Insect. Soc. 61(4), 307–323. https://doi.org/10.1007/s00040-014-0362-6 (2014).Article 

    Google Scholar 
    9.Tartally, A., Szücs, B. & Ebsen, J. R. The first records of Rickia wasmannii Cavara, 1899, a myrmecophilous fungus, and its Myrmica Latreille, 1804 host ants in Hungary and Romania (Ascomycetes: Laboulbeniales, Hymenoptera: Formicidae). Myrmecol. News 10, 123 (2007).
    Google Scholar 
    10.García, F., Espadaler, X., Echave, P. & Vila, R. Hormigas (Hymenoptera, Formicidae) de los acantilados de l’Avenc de Tavertet (Barcelona, Península Ibérica). Boletín de la Sociedad entomológica Aragonesa 47, 363–367 (2010).
    Google Scholar 
    11.Bezdĕčková, K. & Bezdĕčka, P. First records of the myrmecophilous fungus Rickia wasmannii (Ascomycetes: Laboulbeniales) in the Czech Republic. Acta Musei Moraviae Scientiae Biologicae 96(1), 193–197 (2011).
    Google Scholar 
    12.Cavara, F. Di una nuova Laboulbeniacea: Rickia wasmannii, nov. gen. e nov.spec. Malpighia 13(1-2), 173–188. (1899).13.Hulden, L. Floristic notes on palaearctic Laboulbeniales (Ascomycetes). Karstenia 25, 1–16 (1985).Article 

    Google Scholar 
    14.Csata, E., Erős, K. & Markó, B. Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: Changes in host mortality and behavior. Insect. Soc. 61(3), 247–252. https://doi.org/10.1007/s00040-014-0349-3 (2014).Article 

    Google Scholar 
    15.Báthori, F., Csata, E. & Tartally, A. Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae). J. Invertebr. Pathol. 126, 78–82. https://doi.org/10.1016/j.jip.2015.01.005 (2015).Article 
    PubMed 

    Google Scholar 
    16.Báthori, F., Rádai, Z. & Tartally, A. The effect of Rickia wasmannii (Ascomycota, Laboulbeniales) on the aggression and boldness of Myrmica scabrinodis (Hymenoptera, Formicidae). J. Hymenopt. Res. 58, 41. https://doi.org/10.3897/jhr.58.13253 (2017).Article 

    Google Scholar 
    17.Csata, E. et al. Lock-picks: Fungal infection facilitates the intrusion of strangers into ant colonies. Sci. Rep. UK 7(1), 1–14. https://doi.org/10.1038/srep46323 (2017).CAS 
    Article 

    Google Scholar 
    18.Csata, E., Billen, J., Bernadou, A., Heinze, J. & Markó, B. Infection-related variation in cuticle thickness in the ant Myrmica scabrinodis (Hymenoptera: Formicidae). Insect. Soc. 65(3), 503–506. https://doi.org/10.1007/s00040-018-0628-5 (2018).Article 

    Google Scholar 
    19.Tartally, A. et al. Patterns of host use by brood parasitic Maculinea butterflies across Europe. Philos. T. Roy. Soc. B. 374(1769), 20180202. https://doi.org/10.1098/rstb.2018.0202 (2019).Article 

    Google Scholar 
    20.Fauser-Misslin, A., Sadd, B. M., Neumann, P. & Sandrock, C. Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J. Appl. Ecol. 51(2), 450–459. https://doi.org/10.1111/1365-2664.12188 (2014).Article 

    Google Scholar 
    21.Müller, C. B. & Schmid-Hempel, P. Correlates of reproductive success among field colonies of Bombus lucorum: The importance of growth and parasites. Ecol. Entomol. 17, 343–353. https://doi.org/10.1111/j.1365-2311.1992.tb01068.x (1992).Article 

    Google Scholar 
    22.Porter, S. D. Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta. J. Insect Physiol. 34(12), 1127–1133. https://doi.org/10.1016/0022-1910(88)90215-6 (1988).Article 

    Google Scholar 
    23.Nooten, S. S. & Rehan, S. M. Historical changes in bumble bee body size and range shift of declining species. Biodivers. Conserv. 29, 451–467. https://doi.org/10.1007/s10531-019-01893-7 (2020).Article 

    Google Scholar 
    24.Schmid-Hempel, P. On the evolutionary ecology of host–parasite interactions: Addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88, 147–158. https://doi.org/10.1007/s001140100222 (2001).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    25.Molet, M., Péronnet, R., Couette, S., Canovas, C. & Doums, C. Effect of temperature and social environment on worker size in the ant Temnothorax nylanderi. J. Therm. Biol. 67, 22–29. https://doi.org/10.1016/j.jtherbio.2017.04.013 (2017).Article 
    PubMed 

    Google Scholar 
    26.Haelewaters, D., Boer, P., Gort, G. & Noordijk, J. Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants (II): Variation of infection by Rickia wasmannii over habitats and time. Anim. Biol. 65(3–4), 219–231. https://doi.org/10.1163/15707563-00002472 (2015).Article 

    Google Scholar 
    27.Báthori, F., Pfliegler, W. P., Rádai, Z. & Tartally, A. Host age determines parasite load of Laboulbeniales fungi infecting ants: Implications for host-parasite relationship and fungal life history. Mycoscience 30, 1–6. https://doi.org/10.1016/j.myc.2017.09.004 (2017).Article 

    Google Scholar 
    28.Bezdĕčka, P. & Bezdĕčková, K. First record of the myrmecophilous fungus Rickia wasmannii (Ascomycetes: Laboulbeniales) in Slovakia. Folia Faunistica Slovaca 16(2), 71–72 (2011).
    Google Scholar 
    29.Csősz, S. & Majoros, G. Ontogenetic origin of mermithogenic Myrmica phenotypes (Hymenoptera, Formicidae). Insect. Soc. 56, 70–76. https://doi.org/10.1007/s00040-008-1040-3 (2009).Article 

    Google Scholar 
    30.Di Salvo, M. et al. The microbiome of the Maculinea-Myrmica host-parasite interaction. Sci. Rep. UK 9(1), 1–10. https://doi.org/10.1038/s41598-019-44514-7 (2019).ADS 
    CAS 
    Article 

    Google Scholar 
    31.Tragust, S., Tartally, A., Espadaler, X. & Billen, J. Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): Ectoparasitic fungi on ants (Hymenoptera: Formicidae). Myrmecol. News 23, 81–89. https://doi.org/10.25849/myrmecol.news_023:081 (2016).Article 

    Google Scholar 
    32.Konrad, M., Grasse, A. V., Tragust, S. & Cremer, S. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. P. Roy. Soc. B-Biol. Sci. 282(1799), 20141976. https://doi.org/10.1098/rspb.2014.1976 (2015).CAS 
    Article 

    Google Scholar 
    33.Peeters, C., Molet, M., Lin, C. C. & Billen, J. Evolution of cheaper workers in ants: A comparative study of exoskeleton thickness. Biol. J. Linn. Soc. 121, 556–563. https://doi.org/10.1093/biolinnean/blx011 (2017).Article 

    Google Scholar 
    34.Cammaerts-Tricot, M. C. Production and perception of attractive pheromones by differently aged workers of Myrmica rubra (Hymenoptera Formicidae). Insect. Soc. 21(3), 235–247. https://doi.org/10.1007/BF02226916 (1974).Article 

    Google Scholar 
    35.Csősz, S. et al. Insect morphometry is reproducible under average investigation standards. Ecol. Evol. 11(1), 547–559. https://doi.org/10.1002/ece3.7075 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    36.Wolak, M. E., Fairbairn, D. J. & Paulsen, Y. R. Guidelines for estimating repeatability. Methods Ecol. Evol. 3(1), 129–137. https://doi.org/10.1111/j.2041-210X.2011.00125.x (2012).Article 

    Google Scholar 
    37.R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/. R version 4.0.2 (2020-06-22) (Vienna, Austria, 2020).38.Wright, K. nipals: Principal Components Analysis using NIPALS or Weighted EMPCA, with Gram-Schmidt Orthogonalization. R package version 0.7., published 2020-01-24. https://CRAN.R-project.org/package=nipals/index.html (2020).39.Bates, D., Machler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67(1), 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).40.Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. lmerTest package: Tests in linear mixed effects models. J. Stat. Soft. 82(13), 1–26. https://doi.org/10.18637/JSS.V082.I13 (2017).Article 

    Google Scholar 
    41.Fox, J. & Weisberg, S. An R Companion to Applied Regression 3rd edn. (Sage, 2019).
    Google Scholar 
    42.Jennrich, R. I. An asymptotic χ2 test for the equality of two correlation matrices. J. Am. Stat. Assoc. 65(330), 904–912. https://doi.org/10.1080/01621459.1970.10481133 (1970).MathSciNet 
    Article 
    MATH 

    Google Scholar  More

  • in

    Maintaining momentum for collaborative working groups in a post-pandemic world

    The authors acknowledge valuable discussion with other members of the International Synthesis Consortium, including M. de Araujo Mamede, M. Palmer, J. Kramer, R. Beilinson, J. Arnott and P. Kille. J.B. thanks USGS internal reviewers K. Bagstad and W. Sanford. We also acknowledge all synthesis group members who have been incredibly creative in continuing their research dynamic despite going 100% virtual. M.W. acknowledges funding by the DFG (via iDiv: FZT 118, 02548816). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government. More

  • in

    Unpalatable plants induce a species-specific associational effect on neighboring communities

    1.Huang, Y. et al. Foraging responses of sheep to plant spatial micro-patterns can cause diverse associational effects of focal plant at individual and population levels. J. Anim. Ecol. 87, 863–873 (2018).Article 

    Google Scholar 
    2.Suzuki, R. O. & Suzuki, S. N. Facilitative and competitive effects of a large species with defensive traits on a grazing-adapted, small species in a long-term deer grazing habitat. Plant Ecol. 212, 343–351 (2011).Article 

    Google Scholar 
    3.Courant, S. & Fortin, D. Foraging decisions of bison for rapid energy gains can explain the relative risk to neighboring plants in complex swards. Ecology 91, 1841–1849 (2010).Article 

    Google Scholar 
    4.Callaway, R. M., Kikodze, D., Chiboshvili, M. & Khetsuriani, L. Unpalatable plants protect neighbors from grazing and increase plant community diversity. Ecology 86, 1856–1862 (2005).Article 

    Google Scholar 
    5.Barbosa, P. et al. Associational resistance and associational susceptibility: Having right or wrong neighbors. Annu. Rev. Ecol. Evol. Syst. 40, 1–20 (2009).Article 

    Google Scholar 
    6.Graff, P., Aguiar, M. R. & Chaneton, E. J. Shifts in positive and negative plant interactions along a grazing intensity gradient. Ecology 88, 188–199 (2007).Article 

    Google Scholar 
    7.Fidelis, A., Overbeck, G. E., Pillar, V. D. & Pfadenhauer, J. The ecological value of Eryngium horridum in maintaining biodiversity in subtropical grasslands. Austral Ecol. 34, 558–566 (2009).Article 

    Google Scholar 
    8.Uytvanck, J. V., Maes, D., Vandenhaute, D. & Hoffmann, M. Restoration of woodpasture on former agricultural land: The importance of safe sites and time gaps before grazing for tree seedlings. Biol. Conserv. 141, 78–88 (2008).Article 

    Google Scholar 
    9.Yu, F., Krüsi, B., Schütz, M., Schneller, J. & Wildi, O. Is vegetation inside Carex sempervirens tussocks highly specific or an image of the surrounding vegetation?. J. Veg. Sci. 17, 567–576 (2006).Article 

    Google Scholar 
    10.Cheng, W. et al. Unpalatable weed Stellera chamaejasme L. provides biotic refuge for neighboring species and conserves plant diversity in overgrazing alpine meadows on the Tibetan Plateau in China. J. Mt. Sci. 11, 746–754 (2014).Article 

    Google Scholar 
    11.Gao, F. et al. The expansion process of a Stellera chamaejasme population in a degraded alpine meadow of Northwest China. Environ. Sci. Pollut. Res. 26, 20469–20474 (2019).Article 

    Google Scholar 
    12.Hierro, J. L. & Cock, M. C. Herbivore-mediated facilitation alters composition and increases richness and diversity in ruderal communities. Plant Ecol. 214, 1287–1297 (2013).Article 

    Google Scholar 
    13.Wang, L. et al. Spatially complex neighboring relationships among grassland plant species as an effective mechanism of defense against herbivory. Oecologia 164, 193–200 (2010).ADS 
    Article 

    Google Scholar 
    14.Sotomayor, D. A. & Lortie, C. J. Indirect interactions in terrestrial plant communities: Emerging patterns and research gaps. Ecosphere 6, art103 (2015).Article 

    Google Scholar 
    15.Castillo, J. P., Verdú, M. & Valiente-Banuet, A. Neighborhood phylodiversity affects plant performance. Ecology 91, 3656–3663 (2010).Article 

    Google Scholar 
    16.Verwijmeren, M., Smit, C., Bautista, S., Wassen, M. J. & Rietkerk, M. Combined grazing and drought stress alter the outcome of nurse: Beneficiary interactions in a semi-arid ecosystem. Ecosystems 22, 1295–1307 (2019).Article 

    Google Scholar 
    17.Memariani, F., Joharchi, M. R., Ejtehadi, H. & Emadzade, K. A contribution to the flora and vegetation of Binalood mountain range, NE Iran: Floristic and chorological studies in Fereizi region. Ferdowsi Univ. Int. J. Biol. Sci. J. Cell Mol. Res. 1, 1–17 (2009).
    Google Scholar 
    18.Kartoolinezhad, D. & Moshki, A. Changes in Juniperus polycarpos community in response to physiographical factors (Hezarmasjed Mountain, Iran). Austrian J. For. Sci. 4, 215–232 (2014).
    Google Scholar 
    19.Erfanian, M. B., Ejtehadi, H., Vaezi, J. & Moazzeni, H. Plant community responses to multiple disturbances in an arid region of northeast Iran. Land Degrad. Dev. 30, 1554–1563 (2019).Article 

    Google Scholar 
    20.Memariani, F. & Joharchi, M. R. Iris ferdowsii (Iridaceae), a new species of section Regelia from northeast of Iran. Phytotaxa 291, 192 (2017).Article 

    Google Scholar 
    21.Erfanian, M.B., Sagharyan, M., Memariani, F. & Ejtehadi, H. Predicting range shifts of three endangered endemic plants of the Khorassan-Kopet Dagh floristic province under global change. Sci Rep 11, 9159 (2021).22.Erfanian, M. B. et al. Plant community responses to environmentally friendly piste management in northeast Iran. Ecol. Evol. 9, 8193–8200 (2019).Article 

    Google Scholar 
    23.Morteza-Semnani, K., Moshiri, K. & Akbarzadeh, M. The essential oil composition of Phlomis cancellata Bunge. J. Essent. Oil Res. 18, 672–673 (2006).CAS 
    Article 

    Google Scholar 
    24.Atashgahi, Z., Ejtehadi, H., Mesdaghi, M. & Ghasemzadeh, F. Plant diversity of the Heydari Wildlife Refuge in northeastern Iran, with a checklist of vascular plants. Phytotaxa 340, 101–127 (2018).Article 

    Google Scholar 
    25.Arzani, H., Motamedi, J., Aghajanlu, F., Rashtvand, S. & Zareii, A. Forage quality of important rangeland species in mountainous rangelands of Qazvin and Badman Zanjan. J. Range Watershed Manag. 69, 805–818 (2017).
    Google Scholar 
    26.Hosseini, S. S. Study of Plant Biodiversity in Relation to Physiographic Factors in Hezar Masjed Summit, Khorasan Razavi Province, NE Iran. MSc Thesis (Ferdowsi University of Mashhad, 2016) (in Persian).27.Chao, A. et al. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).Article 

    Google Scholar 
    28.Chao, A. & Jost, L. Coverage-based rarefaction and extrapolation: Standardising samples by completeness rather than size. Ecology 93, 2533–2547 (2012).Article 

    Google Scholar 
    29.Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).Article 

    Google Scholar 
    30.Barber, N. A. et al. Grassland restoration characteristics influence phylogenetic and taxonomic structure of plant communities and suggest assembly mechanisms. J. Ecol. 107, 2105–2120 (2019).Article 

    Google Scholar 
    31.Jin, Y. & Qian, H. V. PhyloMaker: An R package that can generate very large phylogenies for vascular plants. Ecography https://doi.org/10.1111/ecog.04434 (2019).Article 

    Google Scholar 
    32.Chao, A., Chiu, C.-H. & Jost, L. Phylogenetic diversity measures based on Hill numbers. Philos. Trans. R. Soc. B Biol. Sci. 365, 3599–3609 (2010).Article 

    Google Scholar 
    33.Chao, A. et al. Rarefaction and extrapolation of phylogenetic diversity. Methods Ecol. Evol. 6, 380–388 (2015).Article 

    Google Scholar 
    34.Legendre, P. & Legendre, L. F. J. Numerical Ecology (Elsevier, 2012).MATH 

    Google Scholar 
    35.Oksanen, J. et al. vegan: Community Ecology Package. R package. https://CRAN.R-project.org/package=vegan (2017).36.R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2019).37.Boughton, E. H., Quintana-Ascencio, P. F. & Bohlen, P. J. Refuge effects of Juncus effusus in grazed, subtropical wetland plant communities. Plant Ecol. 212, 451–460 (2011).Article 

    Google Scholar 
    38.Axelsson, E. P. & Stenberg, J. A. Associational resistance mediates interacting effects of herbivores and competitors on fireweed performance. Basic Appl. Ecol. 15, 10–17 (2014).Article 

    Google Scholar 
    39.Liu, Q. et al. Allelochemicals in the rhizosphere soil of Euphorbia himalayensis. J. Agric. Food Chem. 62, 8555–8561 (2014).CAS 
    Article 

    Google Scholar 
    40.Gholamalipour Alamdari, E., Seifolahi, B., Avarseji, Z. & Biabavi, A. Evaluation of allelopathic effect of Euphorbia maculata weed on traits of germination, chlorophyll and carotenoids pigments of wheat cultivars. Iran. J. Seed Res. 5, 71–85 (2018).Article 

    Google Scholar 
    41.Steenhagen, D. A. & Zimdahl, R. L. Allelopathy of leafy spurge (Euphorbia esula). Weed Sci. 27, 1–3 (1979).Article 

    Google Scholar 
    42.da Silva, U. P., Furlani, G. M., Demuner, A. J., da Silva, O. L. M. & Varejão, E. V. V. Allelopathic activity and chemical constituents of extracts from roots of Euphorbia heterophylla L. Nat. Prod. Res. 33, 2681–2684 (2019).Article 

    Google Scholar 
    43.Miller, A. M., McArthur, C. & Smethurst, P. J. Spatial scale and opportunities for choice influence browsing and associational refuges of focal plants. J. Anim. Ecol. 78, 1134–1142 (2009).Article 

    Google Scholar 
    44.Huang, Y., Wang, L., Wang, D., Zeng, D.-H. & Liu, C. How does the foraging behavior of large herbivores cause different associational plant defenses?. Sci. Rep. 6, 20561 (2016).ADS 
    CAS 
    Article 

    Google Scholar  More

  • in

    The risk reduction effect of sediment production rate by understory coverage rate in granite area mountain forest

    In this study, as shown in the conceptual image described in Fig. 2, we supposed that the cause to promote sediment production rate from forest areas to rivers is understory coverage rate decreasing. As the locations of the survey, we selected three granite low mountain forest areas in Japan; Hiei mountain, Kagami mountain, and Suzuka mountain. These places were the similar environmental conditions, forest woods, understory plants, the incline which almost less than 35°, and the latitude which is N35°04′-05′ at catchments of the river which inflow to Lake Biwa. We surveyed Shiga prefecture where is almost Lake Biwa basin in the western area of Japan. The forest area of Shiga prefecture is about 200,000 ha (about 60% occupied the prefecture area). About 80,000 ha of them are the artificial forest of cedar and cypress. Most of the planted forests are of an age that can be cut down and used. The locations of the field survey, we selected three low mountain forest areas on granite area and almost the same latitude in Lake Biwa basin; Hiei mountain, Kagami mountain, and Suzuka mountain (Fig. 3).Figure 2The concept ecosystem image diagram of the relationship between understory coverage rate and sediment production in the low mountain forest area. The understory disturbs sediments moving. The concept image diagram was drawn by T. Mizuno using Microsoft PowerPoint.Full size imageFigure 3The location map of the field survey forest of the low mountain on granite are between N35 06′ from N35 04′, where are the basin of Lake Biwa near Kyoto in the western area of Japan. The location map was based on the Digital Topographic Map 25,000 published by the Geospatial Information Authority of Japan (https://maps.gsi.go.jp), and was edited and processed by T. Mizuno using Microsoft PowerPoint.Full size imageFor the sediment production rate, annual actual measurement data of sediment receiving boxes, sediment receiving weirs, and dams were used. For the understory coverage rate, the Miura method was used18. The almost physical flow of forest surfaces is expressed in the form of a function of exponentiation19. Therefore, in the meta-analysis of all field data, the Poisson regression analysis (log function) of the generalized linear mixed-effects regression model was used. The dependent variable was the sediment production rate, the explanatory variable was the understory coverage rate and the random effect was the rain intensity. Because the rainfall intensity has a large effect on the surface flow of the forest when the amount of rainfall exceeds 90 (mm) on the moist soil4. Therefore, assuming that the maximum annual rainfall of 72 h is strongly related to sediment movement, it was used as an index of rainfall intensity. All-year data of Hiei, Kagami, and Suzuka of the maximum annual rainfall of 72 h exceeded 90 (mm). The rainfall intensity was categorized 6 levels; 100–200 (mm), 200–300 (mm), 300–400 (mm), 400–500 (mm), 500–600 (mm) and 600–700 (mm). Each rainfall intensity was inserted as the random effect in the Poisson regression analysis model. Statistical analysis software used R20 and performed calculations using the lme4 package21.Detail method of field survey of Hiei mountain forest (St.1)We carried out a field survey on the sediment production rate on a forest slope in the Hiei mountain forest owned by Enryakuji temple which was recorded world heritage. The stream order of the survey site is the zero-order basin of the Omiya River. The survey point was set in the forest of Sakamoto-Cho, Otsu City (Latitude and longitude notation; 35° 5′ 29ʺ N, 135° 50′ 10ʺ E) located in the uppermost stream of the Omiya River in the southwestern part of Shiga Prefecture. The bedrocks were mainly granite rock and the soil was brown forest soil. The altitude was about 760 (m), the slope direction was east, and the slope was 32°–35°. The main forest wood was the Japanese cypress (Chamaecyparis obtusa), which was about 100 years old, and the forest floor was relatively bright with moderate forest density. Besides, dwarf bamboo flourished on the forest floor of the study site and nearby forests until around 2005. At present, there are many areas where understory vegetation has disappeared due to deer feeding damage. At the survey point, the surface of the forest floor had become bare. On the forest slope where the understory vegetation had disappeared, we made a 5.0 (m) × 5.0 (m) survey area surrounded by a protective fence with a height of about 2.0 (m) to prevent deer feeding damage. At the lower end of the survey area, five sediment receiving boxes with a width of 25 (cm) and a height of 15 (cm) were installed at intervals of about 1.0 (m) along the contour lines. The survey started in June 2015, and the samples captured in the sediment receiving box were collected approximately once every two to four weeks, and after heavy rain appropriately. The collected sediment sample was air-dried, dried at 70 °C for 24 h or more, fractionated into sediment and litter, and the weight of each was measured. The sediment production rate was converted with a specific gravity of 1.8 (tons) per 1.0 (m3). As for the understory coverage rate, vegetation growth, litter, sediment, and gravel were evaluated by the point-counting by the Miura method18 in a range of 50 (cm) × 50 (cm) above each sediment receiving a box every autumn. Also, we checked the vegetation overgrowth around the field survey area. As the rainfall data used in the analysis, the observation data (observatory name: Hiei) closest to the survey site was used from the water quality hydrology database of the Ministry of Land, Infrastructure, Transport, and Tourism. The boxplot of the annual sediment production rate (m3/km2/year) was made by using soft-wares R3.6.120.Detail method of field survey of Kagami mountain (St.2)We collected data about the sediment production rate of the forest with 60% or more of the understory coverage rate in the Kagami mountain forest where no deer has been confirmed. The stream order of the survey site was a 0–3 order basin within the catchment area of the Hino River. The investigation point of sediment outflow from the forest was conducted at the forest mountain stream in Oshinohara, Yasu City (Latitude and longitude notation; 35° 4′ 2ʺ N, 136° 4′ 3ʺ E). The bedrock is granite, and the soil is brown forest soil. The catchment area of the study site is 20.0 ha, the altitude is about 150–280 (m), the slope of the mountain stream is north, and the slope of the mountain stream is about 11°. The main forest wood was the Japanese cypress (Chamaecyparis obtusa) and deciduous broad-leaved trees such as oak. No deer feeding damage to adult trees and understory was observed high density in the survey area. Mainly understory is the fern plant (Gleichenia japonica). Now the understory coverage rate is 60% or more anywhere. Sediment and litter that flowed out of the forest were collected from the upper part of the concrete weir (2.4 (m) wide × 1.2 (m) tall) installed at the downstream end of the survey site. We collected approximately once every two to four weeks after heavy rain in five years from 2015 to 2019. The collected sediment sample was air-dried for about 1 week, then dried at 70 °C for 24 h or more, and the weight of gravel and litter was measured. The boxplot of the annual sediment production rate (m3/km2/year) was made by using soft-wares R3.6.120.Detail method of data collection of Suzuka mountain (St.3)We collected data about the sediment production rate of the forest with both cases under 30% and 30%-60% of the understory coverage rate in the Suzuka mountain by using the Eigenji dam annual sediment deposit data. The elevation of the Eigenji Dam dam is 274 (m), and the maximum elevation of the catchment area of the Eigenji Dam is 1247 (m). The Eigenji dam is the stream order which is a 0–6 order basin within the catchment area of the Echi River. The Eigenji Dam was built in 1973 on the Echi River in Higashi-Omi City, Shiga Prefecture (Latitude and longitude notation; 35° 4′ 35ʺ N, 136° 20′ 7ʺ E), the catchment area is 131.5 km2. The catchment area is almost the forest area of the Suzuka mountain. The main bedrock of the Eigenji dam is granite, and the main bedrocks of the catchment are granite and sedimentary rock. The soil is brown forest soil. The slope of the watershed area is 10–20°. The report of Shiga prefecture referred to the damage caused by overgrazing by deer began to increase around 201022,23. In 2011, a large decrease in understory was confirmed in the entire watershed of the Eigenji Dam24. The boxplot of the annual sediment deposition (m3/km2/year) was made by dividing the period’s case 1 is when a 30–60% understory coverage rate from 1982 to 2009 and case 2 is when under 30% understory coverage rate from 2010 to 2015 by using soft-wares R3.6.120.Detail explains of the random effect of the equation of meta-analysisThe Poisson regression analysis (log function) of the generalized linear mixed-effects regression model was used. The dependent variable was the sediment production rate, the explanatory variable was the understory coverage rate and the random effect was the rainfall intensity. The rain intensity was categorized 6 levels; 100–200 (mm), 200–300 (mm), 300–400 (mm), 400–500 (mm), 500–600 (mm) and 600–700 (mm). Each rain intensity was inserted as a random effect in the Poisson mixed-effect regression analysis model. Statistical analysis software used R and performed calculations using the lme4 package21. More

  • in

    Resistance to permethrin alters the gut microbiota of Aedes aegypti

    1.WHO Pesticides and their application for the control of vectors and pests of public health importance. In WHO/CDS/NTD/WHOPES/GCDPP/2006.1 (2006).2.Corbel, V. et al. Multiple insecticide resistance mechanisms in Anopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop. 101, 207–216 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.N’Guessan, R., Corbel, V., Akogbeto, M. & Rowland, M. Reduced efficacy of insecticide-treated nets and indoor residual spraying for malaria control in pyrethroid resistance area, Benin. Emerg. Infect. Dis. 13, 199–206 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Ranson, H. et al. Pyrethroid resistance in African anopheline mosquitoes: What are the implications for malaria control?. Trends Parasitol. 27, 91–98 (2010).PubMed 
    Article 

    Google Scholar 
    5.Chareonviriyaphap, T. et al. Review of insecticide resistance and behavioral avoidance of vectors of human diseases in Thailand. Parasit. Vectors 6, 280 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Liu, N. insecticide resistance in mosquitoes: Impact, mechanisms and research directions. Annu. Rev. Entomol. 60, 537–559 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    7.Dada, N. et al. Pyrethroid exposure alters internal and cuticle surface bacterial communities in Anopheles albimanus. ISME J. 10, 2447–2464 (2019).Article 

    Google Scholar 
    8.Dada, N., Sheth, M., Liebman, K., Pinto, J. & Lenhart, A. Whole metagenome sequencing reveals links between mosquito microbiota and insecticide resistance in malaria vectors. Sci. Rep. 8, 2084 (2018).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.Soltani, A., Vatandoost, H., Oshaghi, M. A., Enayati, A. A. & Chavshin, A. R. The role of midgut symbiotic bacteria in resistance of Anopheles stephensi (Diptera: Culicidae) to organophosphate insecticides. Pathog. Glob. Health 111, 289–296 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Pietri, J.E., Tiffany, C. & Liang, D. Disruption of the microbiota affects physiological and evolutionary aspects of insecticide resistance in the German cockroach, an important urban pest. PLoS One 13, e0207985 (2018).11.Cheng, D. et al. Gut symbiont enhances insecticide resistance in a significant pest, the oriental fruit fly Bactrocera dorsalis (Hendel). Microbiome 5, 13 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Xia, X. et al. DNA sequencing reveals the midgut microbiota of diamondback moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance. PLoS ONE 8, e68852 (2013).13.Xia, X. et al. Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella (L.). Front Microbiol. 9, 25 (2018).14.Kontsedalov, S. et al. The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag. Sci. 64, 789–792 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Ghanim, M. & Kontsedalov, S. Susceptibility to insecticides in the Q biotype of Bemisia tabaci is correlated with bacterial symbiont densities. Pest Manag. Sci. 65, 939–942 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Kikuchi, Y. et al. Symbiont-mediated insecticide resistance. Proc. Natl. Acad. Sci. USA 109, 8618–8622 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.Badolo, A. et al. Insecticide resistance levels and mechanisms in Aedes aegypti populations in and around Ouagadougou, Burkina Faso. PLoS Negl. Trop. Dis. 13, e0007439 (2019).18.Kandel, Y. et al. Widespread insecticide resistance in Aedes aegypti L. from New Mexico, U.S.A. PLoS One 14, e0212693 (2019).19.Amelia-Yap, Z. H., Chen, C. D., Sofian-Azirun, M. & Low, V. L. Pyrethroid resistance in the dengue vector Aedes aegypti in Southeast Asia: Present situation and prospects for management. Parasit. Vectors 11, 332 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Li, W., Jin, D., Shi, C. & Li, F. Midgut bacteria in deltamethrin-resistant, deltamethrin-susceptible, and field-caught populations of Plutella xylostella, and phenomics of the predominant midgut bacterium Enterococcus mundtii. Sci. Rep. 7, 1947 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    21.Barnard, K., Jeanrenaud, A., Brooke, B. D. & Oliver, S. V. The contribution of gut bacteria to insecticide resistance and the life histories of the major malaria vector Anopheles arabiensis (Diptera: Culicidae). Sci. Rep. 9, 9117 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Tetreau, G. et al. Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis. Parasit. Vectors 11, 121 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Aislabie, J. & Lloyd-Jones, G. A review of bacterial degradation of pesticides. Aust. J. Soil Res. 33, 925–942 (1995).CAS 
    Article 

    Google Scholar 
    24.Lien, N. T. K. et al. Transcriptome sequencing and analysis of changes associated with insecticide resistance in the dengue mosquito (Aedes aegypti) in Vietnam. Am. J. Trop. Med. Hyg. 100, 1240–1248 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Berticat, C., Rousset, F., Raymond, M., Berthomieu, A. & Weill, M. High Wolbachia density in insecticide-resistant mosquitoes. Proc. R. Soc. Lond. Ser. B-Biol.l Sci. 269, 1413–1416 (2002).26.Hamada, M., Matar, A. & Bashir, A. Carbaryl degradation by bacterial isolates from a soil ecosystem of the Gaza Strip. Braz. J. Microbiol. 46, 1087–1091 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Akbar, S., Sultan, S. & Kertesz, M. Determination of cypermethrin degradation potential of soil bacteria along with plant growth-promoting characteristics. Curr. Microbiol. 70, 75–84 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Durand, C., Ruban, V., Ambles, A., Clozel, B. & Achard, L. Characterisation of road sediments near Bordeaux with emphasis on phosphorus. J. Environ. Monit. 5, 463–467 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Zehetner, F., Rosenfellner, U., Mentler, A. & Gerzabek, M. H. Distribution of road salt residues, heavy metals and polycyclic aromatic hydrocarbons across a highway-forest interface. Water Air Soil Pollut. 198, 125–132 (2009).ADS 
    CAS 
    Article 

    Google Scholar 
    30.Fuchs, G., Boll, M. & Heider, J. Microbial degradation of aromatic compounds—From one strategy to four. Nat. Rev. Microbiol. 9, 803–816 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Zhu, K. Y., Merzendorfer, H., Zhang, W., Zhang, J. & Muthukrishnan, S. Biosynthesis, turnover, and functions of chitin in insects. Annu. Rev. Entomol. 61, 177–196 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    32.Czaplicka, M. Sources and transformations of chlorophenols in the natural environment. Sci. Total Environ. 322, 21–39 (2004).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    33.Igbinosa, E.O. et al. Toxicological profile of chlorophenols and their derivatives in the environment: The public health perspective. Sci. World J. 2013, 460215 (2013).34.Li, N., Chen, J. M., Zhang, Y. F., He, Y. P. & Chen, L. Z. Comparison for activities of detoxifying enzymes between in resistant-strains and susceptible-imidacloprid endosymbiotic strains of rice brown planthopper, Nilaparvata lugens. Acta Agric. Univ. Zhejiangensis 22, 653–659 (2010).
    Google Scholar 
    35.Dowd, P. F. & Shen, S. K. The contribution of symbiotic yeast to toxin resistance of the cigarette beetle (Lasioderma serricorne). Entomol. Exp. Appl. 56, 241–248 (1990).CAS 
    Article 

    Google Scholar 
    36.Brogdon, W. G. & McAllister, J. C. Simplification of adult mosquito bioassays through use of time-mortality determinations in glass bottles. J. Am. Mosq. Control Assoc. 14, 159–164 (1998).CAS 
    PubMed 

    Google Scholar 
    37.Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516–4522 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Muyzer, G., de Waal, E. C. & Uitterlinden, A. G. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695–700 (1993).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Muturi, E. J., Njoroge, T. M., Dunlap, C. & Caceres, C. E. Blood meal source and mixed blood-feeding influence gut bacterial community composition in Aedes aegypti. Parasit. Vectors 14, 83 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Quast, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    41.Arndt, D. et al. METAGENassist: A comprehensive web server for comparative metagenomics. Nucleic Acids Res. 40, W88–W95 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    42.Hammer, O., Harper, D. A. T. & Ryan, P. D. PAST: Paleontological statistics software package for education and data analysis. Paleontol. Electron. 4, 4–9 (2001).
    Google Scholar 
    43.Bokulich, N. A. et al. Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat. Methods 10, 57–59 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Oksanen, J. et al. vegan: Community Ecology Package. R Package Version 2.3–5. https://CRAN.R-project.org/package=vegan (2016).45.Quinn, G. & Keough, M. Experimental Design and Data Analysis for Biologists (Cambridge University Press, 2002).Book 

    Google Scholar  More

  • in

    Signatures of mitonuclear coevolution in a warbler species complex

    1.Calvo, S. E. & Mootha, V. K. The mitochondrial proteome and human disease. Annu. Rev. Genomics Hum. Genet. 11, 25–44 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Lane, N. Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations. BioEssays 33, 860–869 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Bar-Yaacov, D. et al. Mitochondrial involvement in vertebrate speciation? The case of mito-nuclear genetic divergence in chameleons. Genome Biol. Evol. 7, 3322–3336 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.Hill, G. E. Mitonuclear Ecology (Oxford Univ. Press, 2019).5.Ballard, J. W. O. & Whitlock, M. C. The incomplete natural history of mitochondria. Mol. Ecol. 13, 729–744 (2004).PubMed 
    Article 

    Google Scholar 
    6.Morales, H. E. et al. Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nat. Ecol. Evol. 2, 1258–1267 (2018).PubMed 
    Article 

    Google Scholar 
    7.Hill, G. E. et al. Assessing the fitness consequences of mitonuclear interactions in natural populations. Biol. Rev. 94, 1089–1104 (2019).PubMed 
    Article 

    Google Scholar 
    8.Barreto, F. S. & Burton, R. S. Elevated oxidative damage is correlated with reduced fitness in interpopulation hybrids of a marine copepod. Proc. R. Soc. B Biol. Sci. 280, 20131521 (2013).Article 

    Google Scholar 
    9.Healy, T. M. & Burton, R. S. Strong selective effects of mitochondrial DNA on the nuclear genome. Proc. Natl Acad. Sci. U.S.A. 117, 6616–6621 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    10.Burton, R. S., Pereira, R. J. & Barreto, F. S. Cytonuclear genomic interactions and hybrid breakdown. Annu. Rev. Ecol. Evol. Syst. 44, 281–302 (2013).Article 

    Google Scholar 
    11.Hill, G. E. The mitonuclear compatibility species concept. Auk 134, 393–409 (2017).Article 

    Google Scholar 
    12.Burton, R. S. & Barreto, F. S. A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol. Ecol. 21, 4942–4957 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    13.Weir, J. T. & Schluter, D. Ice sheets promote speciation in boreal birds. Proc. R. Soc. B Biol. Sci. 271, 1881–1887 (2004).Article 

    Google Scholar 
    14.Hewitt, G. M. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68, 87–112 (1999).Article 

    Google Scholar 
    15.Hewitt, G. The genetic legacy of the quaternary ice ages. Nature 405, 907–913 (2000).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Innocenti, P., Morrow, E. H. & Dowling, D. K. Experimental evidence supports a sex-specific selective sieve in mitochondrial genome evolution. Science 332, 845–848 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    17.Harada, A. E., Healy, T. M. & Burton, R. S. Variation in thermal tolerance and its relationship to mitochondrial function across populations of Tigriopus californicus. Front. Physiol. 10, 213 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Acevedo, P. et al. Range dynamics driven by quaternary climate oscillations explain the distribution of introgressed mtDNA of Lepus timidus origin in hares from the Iberian Peninsula. J. Biogeogr. 42, 1727–1735 (2015).Article 

    Google Scholar 
    19.Elgvin, T. O. et al. The genomic mosaicism of hybrid speciation. Sci. Adv. 3, e1602996 (2017).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Schumer, M., Cui, R., Powell, D. L., Rosenthal, G. G. & Andolfatto, P. Ancient hybridization and genomic stabilization in a swordtail fish. Mol. Ecol. 25, 2661–2679 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Rieseberg, L. H. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359–389 (2002).Article 

    Google Scholar 
    22.Barton, N. H. The role of hybridization in evolution. Mol. Ecol. 10, 551–568 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Gagnaire, P. A., Normandeau, E. & Bernatchez, L. Comparative genomics reveals adaptive protein evolution and a possible cytonuclear incompatibility between European and American Eels. Mol. Biol. Evol. 29, 2909–2919 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Sambatti, J. B. M., Ortiz-Barrientos, D., Baack, E. J. & Rieseberg, L. H. Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecol. Lett. 11, 1082–1091 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Baris, T. Z. et al. Evolved genetic and phenotypic differences due to mitochondrial-nuclear interactions. PLoS Genet. 13, e1006517 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    26.Boratyński, Z., Ketola, T., Koskela, E. & Mappes, T. The sex specific genetic variation of energetics in bank voles, consequences of introgression? Evol. Biol. 43, 37–47 (2016).Article 

    Google Scholar 
    27.Rohwer, S. & Wood, C. Three hybrid zones between Hermit and Townsend’s Warblers in Washington and Oregon. Auk 115, 284–310 (1998).Article 

    Google Scholar 
    28.Rohwer, S., Bermingham, E. & Wood, C. Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55, 405–422 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Krosby, M. & Rohwer, S. A 2000 km genetic wake yields evidence for northern glacial refugia and hybrid zone movement in a pair of songbirds. Proc. R. Soc. B Biol. Sci. 276, 615–621 (2009).CAS 
    Article 

    Google Scholar 
    30.Krosby, M. & Rohwer, S. Ongoing movement of the hermit warbler X Townsend’s Warbler Hybrid Zone. PLoS One 5, e14164 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Wang, S. et al. Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species. Evol. Lett. 4–6, 502–515 (2020).Article 

    Google Scholar 
    32.Choi, Y. & Chan, A. P. PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 31, 2745–2747 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Choi, Y., Sims, G. E., Murphy, S., Miller, J. R. & Chan, A. P. Predicting the functional effect of amino acid substitutions and indels. PLoS ONE (2012).34.Murrell, B. et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8, e1002764 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Michaud, E. J. et al. A molecular model for the genetic and phenotypic characteristics of the mouse lethal yellow (Ay) mutation. Proc. Natl Acad. Sci. USA 91, 2562–2566 (1994).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Nadeau, N. J. et al. Characterization of Japanese quail yellow as a genomic deletion upstream of the avian homolog of the mammalian ASIP (agouti) gene. Genetics 178, 777–786 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Wang, S., Rohwer, S., Delmore, K. E. & Irwin, D. E. Cross-decades stability of an avian hybrid zone. J. Evol. Biol. 32, 1242–1251 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Console, L. et al. The link between the mitochondrial fatty acid oxidation derangement and kidney injury. Front. Physiol. 11, 1–7 (2020).Article 

    Google Scholar 
    39.Houten, S. M. & Wanders, R. J. A. A general introduction to the biochemistry of mitochondrial fatty acid β-oxidation. J. Inherit. Metab. Dis. 33, 469–477 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Clemente, F. J. et al. A selective sweep on a deleterious mutation in CPT1A in arctic populations. Am. J. Hum. Genet. 95, 584–589 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Fumagalli, M. et al. Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349, 1343–1347 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Zoladz, J. A. et al. Effect of temperature on fatty acid metabolism in skeletal muscle mitochondria of untrained and endurance-trained rats. PLoS One 12, e0189456 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    43.Atkin, O. K. & Macherel, D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot. 103, 581–597 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Wu, C. I. The genic view of the process of speciation. J. Evolut. Biol. 14, 851–865 (2001).Article 

    Google Scholar 
    45.Via, S. Natural selection in action during speciation. Proc. Natl Acad. Sci. USA 106, 9939–9946 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Nosil, P. A. Ecological Speciation (Oxford Univ. Press, 2012).47.Feder, J. L., Flaxman, S. M., Egan, S. P., Comeault, A. A. & Nosil, P. Geographic mode of speciation and genomic divergence. Annu. Rev. Ecol. Evol. Syst. 44, 73–97 (2013).Article 

    Google Scholar 
    48.Wright, S. Evolution in Mendelian populations. Genetics 16, 97–159 (1931).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, 1930).50.Hartl, D. L. & Clark, A. Principles of Population Genetics (Sinauer Associates, 2007).51.Irwin, D. E. et al. A comparison of genomic islands of differentiation across three young avian species pairs. Mol. Ecol. 27, 4839–4855 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    52.Nam, K., Mugal, C., Nabholz, C., Schielzeth, H. & Wolf, J. B. Molecular evolution of genes in avian genomes. Genome Biol. 11, R68 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    53.Shafer, A. B. A., Cullingham, C. I., Côté, S. D. & Coltman, D. W. Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Mol. Ecol. 19, 4589–4621 (2010).PubMed 
    Article 

    Google Scholar 
    54.Rohwer, S., Bermingham, E. & Wood, C. Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55, 405 (2001).CAS 
    PubMed 
    Article 

    Google Scholar 
    55.Pielou, E. C. After the Ice Age (University of Chicago Press, 1991).56.Bandelt, H. J., Forster, P. & Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Leigh, J. W. & Bryant, D. POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110–1116 (2015).Article 

    Google Scholar 
    58.Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Baiz, M. D., Wood, A. W., Brelsford, A., Lovette, I. J. & Toews, D. P. L. Pigmentation genes show evidence of repeated divergence and multiple bouts of introgression in Setophaga Warblers. Curr. Biol. 31, 1–7 (2021).Article 
    CAS 

    Google Scholar 
    61.Li, H. & Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform. Bioinformatics 26, 589–595 (2010).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    62.McKenna, Aaron et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. (2010).63.Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Zheng, X. et al. A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28, 3326–3328 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.R Core Team (2017). R: a language and environment for statistical computing. R Found. Stat. Comput. Vienna, Austria. R Foundation for Statistical Computing (2017). S0103-6440200400030001566.Raj, A., Stephens, M. & Pritchard, J. K. fastSTRUCTURE: variational inference of population structure in large SNP datasets. Genetics 197, 573–589 (2014).PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    68.Aulchenko, Y. S., Ripke, S., Isaacs, A. & van Duijn, C. M. GenABEL: an R library for genome-wide association analysis. Bioinformatics 23, 1294–1296 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Johnson, M. et al. NCBI BLAST: a better web interface. Nucleic Acids Res. 36, W5–W9 (2008).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    70.Bateman, A. UniProt: A worldwide hub of protein knowledge. Nucleic Acids Res. 47, D506–D515 (2019).Article 
    CAS 

    Google Scholar 
    71.Legendre, P. Numerical Ecology 2nd edn (Elsevier Science, 1998). https://doi.org/10.1017/CBO9781107415324.00472.Korunes, L. K. & Samuk, K. pixy: unbiased estimation of nucleotide diversity and divergence in the presence of missing data. Mol. Ecol. Resour. 21, 1359–1368 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Gompert, Z. & Buerkle, C. A. Bayesian estimation of genomic clines. Mol. Ecol. 20, 2111–2127 (2011).PubMed 
    Article 

    Google Scholar 
    74.Bates, D. M., Maechler, M., Bolker, B. & Walker, S. lme4: linear mixed-effects models using S4 classes. J. Stat. Softw. 67, 48 (2015).Article 

    Google Scholar 
    75.Bernt, M. et al. MITOS: improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69, 313–319 (2013).PubMed 
    Article 

    Google Scholar 
    76.Kearse, M. et al. Geneious. Bioinformatics (Oxford, 2012).77.Woolley, S., Johnson, J., Smith, M. J., Crandall, K. A. & McClellan, D. A. TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 19, 671–672 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    78.McClellan, D. A. & Ellison, D. D. Assessing and improving the accuracy of detecting protein adaptation with the TreeSAAP analytical software. Int. J. Bioinform. Res. Appl. 6, 120–133 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Wang, T., Hamann, A., Spittlehouse, D. L. & Murdock, T. Q. Climate WNA-high-resolution spatial climate data for western North America. J. Appl. Meteorol. Climatol. 51, 16–29 (2012).ADS 
    Article 

    Google Scholar 
    80.Legendre, P. & Legendre, L. Multidimensional quantitative data. in Numerical Ecology 143–194 (Elsevier UK, 2012). More