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    Isotopic evidence that aestivation allows malaria mosquitoes to persist through the dry season in the Sahel

    Adamou, A. et al. The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar. J. 10, 151 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. et al. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J. Exp. Biol. 215, 2013–2021 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. et al. Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. J. Exp. Biol. 214, 2345–2353 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Lehmann, T. et al. Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Am. J. Trop. Med. Hyg. 83, 601–606 (2010).PubMed 
    PubMed Central 

    Google Scholar 
    Yaro, A. S. et al. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 58, 1050–1059 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Omer, S. M. & Cloudsley-Thompson, J. L. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull. World Health Organ. 42, 319 (1970).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Omer, S. M. & Cloudsley-Thompson, J. L. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 217, 879–880 (1968).
    Google Scholar 
    Holstein, M. H. Biology of Anopheles gambiae (1954). World Health Organization.Andrade, C. M. et al. Increased circulation time of Plasmodium falciparum underlies persistent asymptomatic infection in the dry season. Nat. Med. 26, 1929–1940 (2020).CAS 
    PubMed 

    Google Scholar 
    Coulibaly, D. et al. Spatio-temporal dynamics of asymptomatic malaria: bridging the gap between annual malaria resurgences in a Sahelian environment. Am. J. Trop. Med. Hyg. 27, 1761–1769 (2017).
    Google Scholar 
    Gillies, M. & Wilkes, T. A study of the age-composition of populations of Anopheles gambiae Giles and A. funestus Giles in north-eastern Tanzania. Bull. Entomol. Res. 56, 237–262 (1965).CAS 
    PubMed 

    Google Scholar 
    Gillies, M. T. & De Meillon, B. The Anophelinae of Africa south of the Sahara (Ethiopian Zoogeographical Region) (Johannesburg: South African Institute for Medical Research, 1968).Dao, A. et al. Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516, 387–390 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thomson, J. G. Malaria in Nyasaland. Proc. R. Soc. Med. 28, 391–404 (1934).
    Google Scholar 
    Huestis, D. L. et al. Windborne long-distance migration of malaria mosquitoes in the Sahel. Nature 574, 404–408 (2019).CAS 
    PubMed 

    Google Scholar 
    Lambert, B., North, A., Burt, A. & Godfray, H. C. J. The use of driving endonuclease genes to suppress mosquito vectors of malaria in temporally variable environments. Malar. J. 17, 154 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Verhulst, N. O., Loonen, J. A. C. M. & Takken, W. Advances in methods for colour marking of mosquitoes. Parasit. Vectors 6, 200 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Hagler, J. R. & Jackson, C. G. Methods for marking insects: current techniques and future prospects. Annu. Rev. Entomol. 46, 511–543 (2001).CAS 
    PubMed 

    Google Scholar 
    Hamer, G. L. et al. Dispersal of adult culex mosquitoes in an urban West Nile virus hotspot: a mark–capture study incorporating stable isotope enrichment of natural larval habitats. PLoS Negl. Trop. Dis. 8, e2768 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Hamer, G. L. et al. Evaluation of a stable isotope method to mark naturally-breeding larval mosquitoes for adult dispersal studies. J. Med. Entomol. 49, 61–70 (2012).CAS 
    PubMed 

    Google Scholar 
    Opiyo, M. A. et al. Using stable isotopes of carbon and nitrogen to mark wild populations of Anopheles and Aedes mosquitoes in south-eastern Tanzania. PLoS ONE 11, e0159067 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Hood-Nowotny, R., Mayr, L. & Knols, B. Use of carbon-13 as a population marker for Anopheles arabiensis in a sterile insect technique (SIT) context. Malar. J. 5, 6 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Hood-Nowotny, R. & Knols, B. G. J. Stable isotope methods in biological and ecological studies of arthropods. Entomol. Exp. Appl. 124, 3–16 (2007).CAS 

    Google Scholar 
    Hood-Nowotny, R. et al. Intrinsic and synthetic stable isotope marking of tsetse flies. J. Insect Sci. 11, 79 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Atzrodt, J., Derdau, V., Kerr, W. J. & Reid, M. Deuterium- and tritium-labelled compounds: applications in the life sciences. Angew. Chem. Int. Ed. 57, 1758–1784 (2018).CAS 

    Google Scholar 
    Copia, L., Wassenaar, L. I., Terzer-Wassmuth, S., Belachew, D. L. & Araguas-Araguas, L. J. Comparative evaluation of 2H- versus 3H-based enrichment factor determination on the uncertainty and accuracy of low-level tritium analyses of environmental waters. Appl. Radiat. Isot. 176, 109850 (2021).CAS 
    PubMed 

    Google Scholar 
    Begon, M., Harper, J. & Townsend, C. Ecology: Individuals, Populations and Communities (Blackwell Science, 1996).Faiman, R. et al. Marking mosquitoes in their natural larval sites using 2H-enriched water: a promising approach for tracking over extended temporal and spatial scales. Methods Ecol. Evol. 10, 1274–1285 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Florkin, M. Chemical Zoology: Arthropoda Part B (Academic Press, 2014).Hackman, R. H. & Goldberg, M. Studies on chitin VI. The nature of alpha-and beta-chitins. Aust. J. Biol. Sci. 18, 935–946 (1965).CAS 
    PubMed 

    Google Scholar 
    Faiman, R. et al. Quantifying flight aptitude variation in wild Anopheles gambiae in order to identify long-distance migrants. Malar. J. 19, 263 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Huestis, D. L. & Lehmann, T. Ecophysiology of Anopheles gambiae s.l.: persistence in the Sahel. Infect. Genet. Evol. 28, 648–661 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Lehmann, T. et al. Seasonal variation in spatial distributions of Anopheles gambiae in a Sahelian village: evidence for aestivation. J. Med. Entomol. 51, 27–38 (2014).PubMed 

    Google Scholar 
    Costantini, C. et al. Density, survival and dispersal of Anopheles gambiae complex mosquitoes in a West African Sudan savanna village. Med. Vet. Entomol. 10, 203–219 (1996).CAS 
    PubMed 

    Google Scholar 
    Toure, Y. T. et al. Mark–release–recapture experiments with Anopheles gambiae s.l. in Banambani Village, Mali, to determine population size and structure. Med. Vet. Entomol. 12, 74–83 (1998).CAS 
    PubMed 

    Google Scholar 
    Faiman, R. et al. A novel fluorescence and DNA combination for versatile, long-term marking of mosquitoes. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.13592 (2021).Brattström, O., Bensch, S., Wassenaar, L. I., Hobson, K. A. & Åkesson, S. Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography 33, 720–729 (2010).
    Google Scholar 
    Hobson, K. A., Jinguji, H., Ichikawa, Y., Kusack, J. W. & Anderson, R. C. Long-distance migration of the globe skimmer dragonfly to Japan revealed using stable hydrogen (δ 2H) isotopes. Environ. Entomol. 50, 247–255 (2020).
    Google Scholar 
    Schilling, E. G. et al. Phenological and isotopic evidence for migration as a life history strategy in Aeshna canadensis (family: Aeshnidae) dragonflies. Ecol. Entomol. 46, 209–219 (2021).
    Google Scholar 
    Girard, P., Hillaire-Marcel, C. & Oga, M. S. Determining the recharge mode of Sahelian aquifers using water isotopes. J. Hydrol. 197, 189–202 (1997).CAS 

    Google Scholar 
    Gutiérrez-Expósito, C., Ramírez, F., Afán, I., Forero, M. & Hobson, K. A. Toward a deuterium feather isoscape for sub-Saharan Africa: progress, challenges and the path ahead. PLoS ONE https://doi.org/10.1371/journal.pone.0135938 (2015).Lutz, A., Thomas, J. M. & Panorska, A. Environmental controls on stable isotope precipitation values over Mali and Niger, West Africa. Environ. Earth Sci. 62, 1749–1759 (2011).CAS 

    Google Scholar 
    Risi, C. et al. Understanding the Sahelian water budget through the isotopic composition of water vapor and precipitation. J. Geophys. Res. Atmos. 115, 1–23 (2010).
    Google Scholar 
    Tremoy, G. et al. A 1-year long δ18O record of water vapor in Niamey (Niger) reveals insightful atmospheric processes at different timescales. Geophys. Res. Lett. 39, 1–5 (2012).
    Google Scholar 
    Terzer‐Wassmuth, S., Wassenaar, L. I., Welker, J. M., Araguás-Araguás, L. J. Improved high‐resolution global and regionalized isoscapes of δ18O, δ2H and d‐excess in precipitation. Hydrol. Process. 35 (2021).Hobson, K. A. et al. A multi-isotope (δ13C, δ15N, δ2H) feather isoscape to assign Afrotropical migrant birds to origins. Ecosphere 3, art44 (2012).
    Google Scholar 
    Diuk-Wasser, M. A. et al. Effect of rice cultivation patterns on malaria vector abundance in rice-growing villages in Mali. Am. J. Trop. Med. Hyg. 76, 869–874 (2007).PubMed 

    Google Scholar 
    Sogoba, N. et al. Malaria transmission dynamics in Niono, Mali: the effect of the irrigation systems. Acta Trop. 101, 232–240 (2007).PubMed 

    Google Scholar 
    Florio, J. et al. Diversity, dynamics, direction, and magnitude of high-altitude migrating insects in the Sahel. Sci. Rep. 10, 20523 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wilkins, E. E., Howell, P. I. & Benedict, M. Q. IMP PCR primers detect single nucleotide polymorphisms for Anopheles gambiae species identification, Mopti and Savanna rDNA types, and resistance to dieldrin in Anopheles arabiensis. Malar. J. 5, 125 (2006).PubMed 
    PubMed Central 

    Google Scholar 
    Wassenaar, L. I. & Hobson, K. A. Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ. Health Stud. 39, 211–217 (2003).CAS 
    PubMed 

    Google Scholar 
    Chesson, L. A., Podlesak, D. W., Cerling, T. E. & Ehleringer, J. R. Evaluating uncertainty in the calculation of non-exchangeable hydrogen fractions within organic materials. Rapid Commun. Mass Spectrom. 23, 1275–1280 (2009).CAS 
    PubMed 

    Google Scholar 
    Schimmelmann, A. Determination of the concentration and stable isotopic composition of nonexchangeable hydrogen in organic matter. Anal. Chem. 63, 2456–2459 (1991).CAS 

    Google Scholar 
    Speakman, J. Doubly Labelled Water: Theory and Practice (Chapman & Hall, 1997).Base SAS 9.4 Procedures Guide (SAS Institute, 2015).Cade, B. S. & N, B. R. A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1, 412–420 (2003).
    Google Scholar 
    SAS/STAT® 15.1 User’s Guide (SAS Institute, 2018).Mcclintock, B. T. et al. Uncovering ecological state dynamics with hidden Markov models. Ecol. Lett. 23, 1878–1903 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Issam, M., Naulet, N., Martin, M. L. & Martin, G. J. A site-specific and multielement approach to the determination of liquid–vapor isotope fractionation parameters: the case of alcohols. J. Phys. Chem. 94, 8303–8309 (1990).
    Google Scholar 
    Linderstrøm-Lang, C. U. & Vaslow, F. Isotope effect on the vapor pressures of water–ethanol and deuterium oxide–ethanol-d mixtures. J. Phys. Chem. 72, 2645–2650 (1968).
    Google Scholar 
    Ventura, M. & Jeppesen, E. Effects of fixation on freshwater invertebrate carbon and nitrogen isotope composition and its arithmetic correction. Hydrobiologia 632, 297–308 (2009).CAS 

    Google Scholar  More

  • in

    Unique thermal sensitivity imposes a cold-water energetic barrier for vertical migrators

    Robison, B. H. Conservation of deep pelagic biodiversity. Conserv. Biol. 23, 847–858 (2009).
    Google Scholar 
    Fernandez-Alamo, M. A. & Färber-Lorda, J. Zooplankton and the oceanography of the eastern tropical Pacific: a review. Prog. Oceanogr. 69, 318–359 (2006).
    Google Scholar 
    Bianchi, D., Galbraith, E. D., Carozza, D. A., Mislan, K. A. S. & Stock, C. A. Intensification of open-ocean oxygen depletion by vertically migrating animals. Nat. Geosci. 6, 545–548 (2013).CAS 

    Google Scholar 
    Steinberg, D. K. & Landry, M. R. Zooplankton and the ocean carbon cycle. Annu. Rev. Mar. Sci. 9, 413–444 (2017).
    Google Scholar 
    Kiko, R. & Hauss, H. On the estimation of zooplankton-mediated active fluxes in oxygen minimum zones regions. Front. Mar. Sci. https://doi.org/10.3389/fmars.2019.00741 (2019).Longhurst, A., Bedo, A., Harrison, W., Head, E. & Sameoto, D. Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep Sea Res. Part I 37, 685–694 (1990).CAS 

    Google Scholar 
    Elder, L. E. & Seibel, B. A. The thermal stress response to diel vertical migration in the hyperiid amphipod, Phronima sedentaria. Comp. Biochem. Physiol. A 187, 20–26 (2015).CAS 

    Google Scholar 
    Tremblay, N., Gomez-Gutierrez, J., Zenteno-Savin, T., Robinson, C. J. & Sanchez-Velascoa, L. Role of oxidative stress in seasonal and daily vertical migration of three krill species in the Gulf of California. Limnol. Oceanogr. 55, 2570–2584 (2010).CAS 

    Google Scholar 
    Lopes, A. R. et al. Oxidative stress in deep scattering layers: heat shock response and antioxidant enzymes activities of myctophid fishes thriving in oxygen minimum zones. Deep Sea Res. Part I 82, 10–16 (2013).CAS 

    Google Scholar 
    Seibel, B. A., Schneider, J., Kaartvedt, S., Wishner, K. F. & Daly, K. L. Hypoxia tolerance and metabolic suppression in oxygen minimum zone euphausiids: implications for ocean deoxygenation and biogeochemical cycles. Integr. Comp. Biol. https://doi.org/10.1093/icb/icw091 (2016).Seibel, B. A. et al. Metabolic suppression during protracted exposure to hypoxia in the jumbo squid, Dosidicus gigas, living in an oxygen minimum zone. J. Exp. Biol. 217, 2710–2716 (2014).
    Google Scholar 
    Wishner, K. F. et al. Ocean deoxygenation and zooplankton: very small oxygen differences matter. Sci. Adv. 4, eaau5180 (2018).CAS 

    Google Scholar 
    Koslow, J. A., Goericke, R., Lara-Lopez, A. & Watson, W. Impact of declining intermediate-water oxygen on deepwater fishes in the California Current. Mar. Ecol. Prog. Ser. 436, 207–218 (2011).
    Google Scholar 
    Oschlies, A. A committed fourfold increase in ocean oxygen loss. Nat. Commun. 12, 2307 (2021).CAS 

    Google Scholar 
    Wishner, K. F., Seibel, B. A. & Outram, D. Ocean deoxygenation and copepods: coping with oxygen minimum zone variability. Biogeosciences 17, 2315–2339 (2020).
    Google Scholar 
    Stramma, L. et al. Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nat. Clim. Change 2, 33–37 (2012).CAS 

    Google Scholar 
    Köhn, E. E., Münnich, M., Vogt, M., Desmmet, F. & Gruber, N. Strong habitat compression by extreme shoaling events of hypoxic waters in the Eastern Pacific. J. Geophys. Res. Oceans 127, e2022JC018429 (2022).
    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).
    Google Scholar 
    Pinsky, M. L., Selden, R. L. & Kitchel, Z. J. Climate-driven shifts in marine species ranges: scaling from organisms to communities. Annu. Rev. Mar. Sci. 12, 153–179 (2020).
    Google Scholar 
    Cavole, L. M. et al. Biological impacts of the 2013–2015 warm-water anomaly in the northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016).
    Google Scholar 
    Lavaniegosa, B. E., Jiménez-Herrera, M. A. & Ambriz-Arreola, I. Unusually low euphausiid biomass during the warm years of 2014–2016 in the transition zone of the California Current. Deep Sea Res. Part II 1, 69–170 (2019).
    Google Scholar 
    Lilly, L. E. & Ohman, M. D. Euphausiid spatial displacements and habitat shifts in the southern California Current system in response to El Niño variability. Prog. Oceanogr. 193, 102544 (2021).
    Google Scholar 
    Zeidberg, L. D. & Robison, B. H. Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proc. Natl Acad. Sci. USA 104, 12948–12950 (2007).CAS 

    Google Scholar 
    Szesciorka, A. R. et al. Timing is everything: drivers of interannual variability in blue whale migration. Sci. Rep. 10, 7710 (2020).CAS 

    Google Scholar 
    Hoving, H.-J. et al. Extreme plasticity in life‐history strategy allows a migratory predator (jumbo squid) to cope with a changing climate. Glob. Change Biol. 19, 2089–2103 (2013).
    Google Scholar 
    Boscolo-Galazzo, F. et al. Temperature controls carbon cycling and biological evolution in the ocean twilight zone. Science 371, 1148–1152 (2021).CAS 

    Google Scholar 
    Deutsch, C., Ferrel, A., Seibel, B. A., Pörtner, H.-O. & Huey, R. B. Climate change tightens a metabolic constraint on marine habitats. Science 348, 1132–1135 (2015).CAS 

    Google Scholar 
    Seibel, B. A. & Deutsch, C. Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature. J. Exp. Biol. 223, jeb210492 (2020).
    Google Scholar 
    Deutsch, C., Penn, J. L. & Seibel, B. A. Diverse hypoxia and thermal tolerances shape biogeography of marine animals. Nature 585, 557–562 (2020).CAS 

    Google Scholar 
    Childress, J. J. Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol. Evol. 10, 30–36 (1995).CAS 

    Google Scholar 
    Seibel, B. A. & Drazen, J. C. The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos. Trans. R. Soc. B. 362, 2061–2078 (2007).CAS 

    Google Scholar 
    Seibel, B. A. et al. Oxygen supply capacity breathes new life into the critical oxygen partial pressure (Pcrit). J. Exp. Biol. 224, jeb242210 (2021).
    Google Scholar 
    Childress, J. J. & Seibel, B. A. Life at stable low oxygen: adaptations of animals to oceanic oxygen minimum layers. J. Exp. Biol. 201, 1223–1232 (1998).CAS 

    Google Scholar 
    Garcia, H. E., et al. World Ocean Atlas 2018, Volume 3: Dissolved Oxygen, Apparent Oxygen Utilization, and Oxygen Saturation (NOAA/NESDIS, 2019).Locarnini, R. A., et. al. World Ocean Atlas 2018, Volume 1: Temperature (NOAA/NESDIS, 2019).Maas, A. E., Frazar, S., Outram, D., Seibel, B. A. & Wishner, K. F. Fine-scale vertical distribution of macroplankton and micronekton in an eastern tropical North Pacific in association with an oxygen minimum zone. J. Plankton Res. 36, 1557–1575 (2014).
    Google Scholar 
    Rosa, R. & Seibel, B. A. Synergistic effect of climate-related variables suggests future physiological impairment in a top oceanic predator. Proc. Natl Acad. Sci. USA 52, 20776–20780 (2008).
    Google Scholar 
    Halsey, L. G., Killen, S. S., Clark, T. D. & Norin, T. Exploring key issues of aerobic scope interpretation in ectotherms: absolute versus factorial. Rev. Fish. Biol. Fish. 28, 405–415 (2018).
    Google Scholar 
    Peterson, C. C., Nagy, K. A. & Diamond, J. Sustained metabolic scope. Proc. Natl Acad. Sci. USA 87, 2324–2328 (1990).CAS 

    Google Scholar 
    Seibel, B. A., Luu, B. E., Tessier, S. N., Towanda, T. & Storey, K. B. Metabolic suppression in the pelagic crab, Pleuroncodes planipes, in oxygen minimum zones. Comp. Biochem. Physiol. A 224, 88–97 (2018).CAS 

    Google Scholar 
    Hadj-Moussa, H., Logan, S. M., Seibel, B. A. & Storey, K. B. Potential role for microRNA in regulating hypoxia-induced metabolic suppression in the jumbo squid? BBA Gene Regul. Mech. 1861, 586–593 (2018).CAS 

    Google Scholar 
    Torres, J. J. & Childress, J. J. Relationship of oxygen consumption to swimming speed in Euphausia pacifica. Mar. Biol. 74, 79–86 (1983).
    Google Scholar 
    Cohen, J. H. & Forward, R. B. Jr. Zooplankton diel vertical migration—a review of proximate control. Oceanogr. Mar. Biol. Annu. Rev. 47, 77–110 (2009).
    Google Scholar 
    Gilly, W. F. et al. Locomotion and behavior of Humboldt squid, Dosidicus gigas, in relation to natural hypoxia in the Gulf of California, Mexico. J. Exp. Biol. 215, 3175–3190 (2012).
    Google Scholar 
    Jaffe, J. S., Ohman, M. D. & De Robertis, A. Sonar estimates of daytime activity levels of Euphausia pacifica in Saanich inlet. Can. J. Fish. Aquat. Sci. 56, 2000–2010 (1999).
    Google Scholar 
    Klevjer, T. A. & Kaartvedt, S. Krill (Meganyctiphanes norvegica) swim faster at night. Limnol. Oceanogr. 56, 765–774 (2011).
    Google Scholar 
    Backus, R. H. et al. Ceratoscopelus maderensis: pecuiiar sound-scattering layer identified with this myctophid fish. Science 160, 991–993 (1968).CAS 

    Google Scholar 
    Barham, E. G. in Proceedings of an International Symposium on Biological Sound Scattering in the Ocean (ed. Farquhar, G. B.) 100–118 (Superintendent of Documents, 1971).Sanders, N. K. & Childress, J. J. A comparison of the respiratory function of the haemocyanins of vertically migrating and non-migrating pelagic, deep-sea Oplophorid shrimps. J. Exp. Biol. 152, 167–187 (1990).
    Google Scholar 
    Seibel, B. A. Critical depth in the jumbo squid, Dosidicus gigas (Ommastrephidae), living in oxygen minimum zones II. Blood-oxygen binding. Deep Sea Res. Part II 95, 139–144 (2013).CAS 

    Google Scholar 
    Pörtner, H.-O., Bock, C. & Mark, F. C. Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology. J. Exp. Biol. 220, 2685–2696 (2017).
    Google Scholar 
    Laffoley, D. & Baxter, J. M. Ocean Deoxygenation: Everyone’s Problem—Causes, Impacts, Consequences and Solutions (IUCN, 2019).Birk, M. A. Respirometry: Tools for Conducting and Analyzing Respirometry Experiments. R version 1.4.0 http://cran.r-project.org/package=respirometry (2021).Huang, B. et al. Improvements of the daily optimum interpolation sea surface temperature (DOISST) Version 2.1. J. Clim. 34, 2923–2939 (2021).
    Google Scholar  More

  • in

    Condition- and context-dependent variation of sexual dimorphism across lizard populations at different spatial scales

    Andersson, M. Sexual Selection. (Princeton University Press, 1994).Darwin, C. The Descent of Man and Selection in Relation to Sex. (1871).Bonduriansky, R. The evolution of condition-dependent sexual dimorphism. Am. Nat. 169, 9–19 (2007).PubMed 

    Google Scholar 
    Bonduriansky, R. & Rowe, L. Sexual selection, genetic architecture, and the condition dependence of body shape in the sexually dimorphic fly Prochyliza xanthostoma (Piophilidae). Evolution (NY). 59, 138 (2005).
    Google Scholar 
    Godin, J. G. J. & McDonough, H. E. Predator preference for brightly colored males in the guppy: A viability cost for a sexually selected trait. Behav. Ecol. 14, 194–200 (2003).
    Google Scholar 
    Emlen, D. J., Warren, I. A., Johns, A., Dworkin, I. & Lavine, L. C. A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 80(337), 860–864 (2012).ADS 

    Google Scholar 
    Cothran, R. D. & Jeyasingh, P. D. Condition dependence of a sexually selected trait in a crustacean species complex: Importance of the ecological context. Evolution (NY). 64, 2535–2546 (2010).
    Google Scholar 
    Jakob, E. M., Marshall, S. D. & Uetz, G. W. Estimating fitness: A comparison of body condition indices. Oikos 77, 61 (1996).
    Google Scholar 
    Galeotti, P., Sacchi, R., Pellitteri-Rosa, D. & Fasola, M. The yellow cheek-patches of the Hermann’s tortoise (Reptilia, Chelonia): Sexual dimorphism and relationship with body condition. Ital. J. Zool. 78, 464–470 (2011).
    Google Scholar 
    Sacchi, R. et al. Context-dependent expression of sexual dimorphism in island populations of the common wall lizard (Podarcis muralis). Biol. J. Linn. Soc. 114, 552–565 (2015).
    Google Scholar 
    Greenberg, R. & Olsen, B. Bill size and dimorphism in tidal-marsh sparrows: Island-like processes in a continental habitat. Ecology 91, 2428–2436 (2010).PubMed 

    Google Scholar 
    Clarke, A. Costs and consequences of evolutionary temperature adaptation. Trends Ecol. Evol. 18, 573–581 (2003).
    Google Scholar 
    Stillwell, R. C. & Fox, C. W. Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: Local adaptation versus phenotypic plasticity. Oikos 118, 703–712 (2009).
    Google Scholar 
    García-Roa, R., Garcia-Gonzalez, F., Noble, D. W. A. & Carazo, P. Temperature as a modulator of sexual selection. Biol. Rev. 95, 1607–1629 (2020).PubMed 

    Google Scholar 
    Ficetola, G. F. et al. Ecogeographical variation of body size in the newt Triturus carnifex : Comparing the hypotheses using an information-theoretic approach. Glob. Ecol. Biogeogr. 19, 485–495 (2010).
    Google Scholar 
    Avramo, V. et al. Evaluating the island effect on phenotypic evolution in the Italian wall lizard, Podarcis siculus (Reptilia: Lacertidae). Biol. J. Linn. Soc. 132, 655–665 (2021).
    Google Scholar 
    Simmons, L. W., Lüpold, S. & Fitzpatrick, J. L. Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol. Evol. 32, 964–976 (2017).PubMed 

    Google Scholar 
    Cox, R. M., Skelly, S. L. & John-Alder, H. B. A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution (NY). 57, 1653–1669 (2003).
    Google Scholar 
    Kaliontzopoulou, A., Carretero, M. A. & Llorente, G. A. Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis Lizards. J. Morphol. 268, 152–165 (2007).PubMed 

    Google Scholar 
    Olsson, M., Shine, R., Wapstra, E., Ujvari, B. & Madsen, T. Sexual dimorphism in lizard body shape: The roles of sexual selection and fecundity selection. Evolution (NY). 56, 1538–1542 (2002).
    Google Scholar 
    Zuffi, M. A. L., Casu, V. & Marino, S. The Italian wall lizard, Podarcis siculus, along the Tuscanian coast of central Italy: Biometrical features and phenotypic patterns. Herpetol. J. 22, 207–212 (2012).
    Google Scholar 
    Corti, C., Biaggini, M. & Capula, M. Podarcis siculus (Rafinesque-Schmaltz, 1810). In: Corti, C., Capula, M., Luiselli, L., Razzetti, E., Sindaco, R. Fauna d’Italia: Reptilia (ed. Calderini) 407–417 (2011).Silva-Rocha, I. R., Salvi, D., Carretero, M. A. & Ficetola, G. F. Alien reptiles on Mediterranean Islands: A model for invasion biogeography. Divers. Distrib. 25, 995–1005 (2019).
    Google Scholar 
    Butler, M. A. & Losos, J. B. Multivariate sexual dimorphism, sexual selection, and adaptation in greater antillean Anolis lizards. Ecol. Monogr. 72, 541–559 (2002).
    Google Scholar 
    Kaliontzopoulou, A., Carretero, M. A. & Llorente, G. A. Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: Joining linear and geometric morphometrics. Biol. J. Linn. Soc. 93, 111–124 (2008).
    Google Scholar 
    Herrel, A., Damme, R. V., Vanhooydonck, B. & Vree, F. D. The implications of bite performance for diet in two species of lacertid lizards. Can. J. Zool. 79, 662–670 (2001).
    Google Scholar 
    Lomolino, M. V. Body size evolution in insular vertebrates: generality of the island rule. J. Biogeogr. 32, 1683–1699 (2005).
    Google Scholar 
    Millien, V. Morphological evolution is accelerated among island mammals. PLoS Biol. 4, 1863–1868 (2006).
    Google Scholar 
    de Amorim, M. E. et al. Lizards on newly created islands independently and rapidly adapt in morphology and diet. Proc. Natl. Acad. Sci. U. S. A. 114, 8812–8816 (2017).ADS 

    Google Scholar 
    Madsen, T. & Shine, R. Phenotypic plasticity in body sizes and sexual size dimorphism in European grass snakes. Evolution (NY). 47, 321–325 (1993).
    Google Scholar 
    Levis, N. A., Isdaner, A. J. & Pfennig, D. W. Morphological novelty emerges from pre-existing phenotypic plasticity. Nat. Ecol. Evol. 2, 1289–1297 (2018).PubMed 

    Google Scholar 
    Cox, R. M., Barrett, M. M. & John-Alder, H. B. Effects of food restriction on growth, energy allocation, and sexual size dimorphism in Yarrow’s Spiny Lizard Sceloporus jarrovii. Can. J. Zool. 86, 268–276 (2008).
    Google Scholar 
    Cox, R. M. & Calsbeek, R. Sex-specific selection and intraspecific variation in sexual size dimorphism. Evolution (NY). 64, 798–809 (2010).
    Google Scholar 
    Cox, R. M., Zilberman, V. & John-Alder, H. B. Environmental sensitivity of sexual size dimorphism: Laboratory common garden removes effects of sex and castration on lizard growth. Funct. Ecol. 20, 880–888 (2006).
    Google Scholar 
    Wiens, J. J. & Tuschhoff, E. Songs versus colours versus horns: what explains the diversity of sexually selected traits?. Biol. Rev. 95, 847–864 (2020).PubMed 

    Google Scholar 
    Sivan, J. et al. Relative tail length correlates with body condition in male but not in female crowned leafnose snakes (Lytorhynchus diadema). Sci. Rep. 10, 4130 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Evans, K. L., Greenwood, J. J. D. & Gaston, K. J. Dissecting the species-energy relationship. Proc. R. Soc. B Biol. Sci. 272, 2155–2163 (2005).
    Google Scholar 
    Weier, J. & Herring, D. Measuring vegetation (NDVI & EVI). NASA. https://earthobservatory.nasa.gov/Features/MeasuringVegetation/. (2000).Peñalver-Alcázar, M., Galán, P. & Aragón, P. Assessing Rensch’s rule in a newt: Roles of primary productivity and conspecific density in interpopulation variation of sexual size dimorphism. J. Biogeogr. 46, 2558–2569 (2019).
    Google Scholar 
    Thorpe, R. S. & Baez, M. Geographic variation within an island: univariate and multivariate contouring of scalation, size, and shape of the lizard Gallotia galloti. Evolution (NY). 41, 256–268 (1987).
    Google Scholar 
    Lazić, M. M., Carretero, M. A., Crnobrnja-Isailović, J. & Kaliontzopoulou, A. Effects of environmental disturbance on phenotypic variation: An integrated assessment of canalization, developmental stability, modularity, and allometry in lizard head shape. Am. Nat. 185, 44–58 (2015).PubMed 

    Google Scholar 
    Sagonas, K. et al. Insularity affects head morphology, bite force and diet in a Mediterranean lizard. Biol. J. Linn. Soc. 112, 469–484 (2014).
    Google Scholar 
    MacArthur, R. H. & Wilson, E. O. The theory of island biogeography. (Princeton University Press, 1967).Alzate, A., Etienne, R. S. & Bonte, D. Experimental island biogeography demonstrates the importance of island size and dispersal for the adaptation to novel habitats. Glob. Ecol. Biogeogr. 28, 238–247 (2019).
    Google Scholar 
    Wieser, W. Effects of temperature on ectothermic organisms (Springer, 1973).
    Google Scholar 
    Lucchi, F., Peccerillo, A., Keller, J., Tranne, C. A. & Rossi, P. L. The Aeolian Islands Volcanoes. (Geological Society, 2013).Meiri, S. Evolution and ecology of lizard body sizes. Glob. Ecol. Biogeogr. 17, 724–734 (2008).
    Google Scholar 
    Rohlf, F. J. TpsUtil version 1.87. (2021).Rohlf, F. J. TpsDig2 version 2.31. (2018).Sheets, H. D. CoordGen8. Integrated Morphometrics Package Suite (IMP) 8. (2014).Sheets, H. D. PCAGen8. Integrated Morphometrics Package Suite (IMP) 8. (2014).Lovich, J. E. & Gibbons, J. W. Review of techniques for quantifying sexual size dimorphism. Growth, Dev. Aging 56, 269–281 (1992).Bittinger, K. usedist: Distance Matrix Utilities. (2020).Schulte-Hostedde, A. I., Zinner, B., Millar, J. S. & Hickling, G. J. Restitution of mass-size residuals: Validating body condition indices. Ecology 86, 155–163 (2005).
    Google Scholar 
    Corti, C., Capula, M., Luiselli, L., Razzetti, E. & Sindaco, R. Fauna d’Italia, vol. XLV, Reptilia. (Calderini, 2011).Ermida, S. L., Soares, P., Mantas, V., Göttsche, F. M. & Trigo, I. F. Google earth engine open-source code for land surface temperature estimation from the landsat series. Remote Sens. 12, 1–21 (2020).
    Google Scholar 
    Porter, W. P. Temperature, activity, and lizard life histories. Am. Nat. 142, 273–295 (1993).PubMed 

    Google Scholar 
    Angilletta, M. J., Hill, T. & Robson, M. A. Is physiological performance optimized by thermoregulatory behavior? A case study of the eastern fence lizard Sceloporus undulatus. J. Therm. Biol. 27, 199–204 (2002).
    Google Scholar 
    Aybar, C., Wu, Q., Bautista, L., Yali, R. & Barja, A. rgee: An R package for interacting with Google Earth Engine. J. Open Source Softw. 5, 2272 (2020).ADS 

    Google Scholar 
    Bonardi, A. et al. ReptIslands: Mediterranean islands and the distribution of their reptile fauna. Glob. Ecol. Biogeogr. https://doi.org/10.1111/geb.13490 (2022).Article 

    Google Scholar 
    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference, A Practical Information-Theoretic Approach, Second Edition. (Springer, 2002).Richards, S. A., Whittingham, M. J. & Stephens, P. A. Model selection and model averaging in behavioural ecology: The utility of the IT-AIC framework. Behav. Ecol. Sociobiol. 65, 77–89 (2011).
    Google Scholar 
    Lukacs, P. M. et al. Concerns regarding a call for pluralism of information theory and hypothesis testing. J. Appl. Ecol. 44, 456–460 (2007).
    Google Scholar 
    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).
    Google Scholar 
    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).
    Google Scholar 
    Breheny, P. & Burchett, W. Visualization of regression models using visreg. R J. 9, 56–71 (2017).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing. (2021).QGIS Development Team. QGIS Geographic Information System, version 3.20.1. Open Source Geospatial Foundation Project. http://qgis.osgeo.org. (2022). More

  • in

    High-resolution phylogenetic and population genetic analysis of microbial communities with RoC-ITS

    Srivastava AK, Schlessinger D. Mechanism and regulation of bacterial ribosomal RNA processing. Annu Rev Microbiol. 1990;44:105–29.PubMed 

    Google Scholar 
    Brewer TE, Albertsen M, Edwards A, Kirkegaard RH, Rocha EPC, Fierer N. Unlinked rRNA genes are widespread among bacteria and archaea. ISME J. 2020;14:597–608.PubMed 

    Google Scholar 
    Apirion D, Miczak A. RNA processing in prokaryotic cells. Bioessays. 1993;15:113–20.PubMed 

    Google Scholar 
    Espejo RT, Plaza N. Multiple ribosomal RNA operons in bacteria; their concerted evolution and potential consequences on the rate of evolution of their 16S rRNA. Front Microbiol. 2018;9:1232.PubMed 
    PubMed Central 

    Google Scholar 
    Roller BRK, Stoddard SF, Schmidt TM. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat Microbiol. 2016;1:16160.PubMed 
    PubMed Central 

    Google Scholar 
    Lim K, Furuta Y, Kobayashi I. Large variations in bacterial ribosomal RNA Genes. Mol Biol Evol. 2012;29:2937–48.PubMed 
    PubMed Central 

    Google Scholar 
    Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, et al. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis. 1998;19:554–68.PubMed 

    Google Scholar 
    Woese CR, Fox GE. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci. 1977;74:5088 LP–5090.
    Google Scholar 
    Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci. 1985;82:6955 LP–6959.
    Google Scholar 
    Park YH, Hori H, Suzuki K, Osawa S, Komagata K. Phylogenetic analysis of the coryneform bacteria by 5S rRNA sequences. J Bacteriol. 1987;169:1801–6.PubMed 
    PubMed Central 

    Google Scholar 
    Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J. 5S Ribosomal RNA Database. Nucleic Acids Res. 2002;30:176–8.PubMed 
    PubMed Central 

    Google Scholar 
    Pace NR. The small things can matter. PLoS Biol. 2018;16:e3000009.PubMed 
    PubMed Central 

    Google Scholar 
    Gürtler V. The role of recombination and mutation in 16S–23S rDNA spacer rearrangements. Gene. 1999;238:241–52.PubMed 

    Google Scholar 
    Snyder AK, Adkins KZ, Rio RVM. Use of the internal transcribed spacer (ITS) regions to examine symbiont divergence and as a diagnostic tool for sodalis-related bacteria. Insects. 2011;2:515–31.PubMed 
    PubMed Central 

    Google Scholar 
    Man SM, Kaakoush NO, Octavia S, Mitchell H. The internal transcribed spacer region, a new tool for use in species differentiation and delineation of systematic relationships within the Campylobacter genus. Appl Environ Microbiol. 2010;76:3071–81.PubMed 
    PubMed Central 

    Google Scholar 
    Liguori AP, Warrington SD, Ginther JL, Pearson T, Bowers J, Glass MB, et al. Diversity of 16S-23S rDNA Internal Transcribed Spacer (ITS) reveals phylogenetic relationships in Burkholderia pseudomallei and its near-neighbors. PLoS One. 2011;6:e29323.PubMed 
    PubMed Central 

    Google Scholar 
    Boyer SL, Flechtner VR, Johansen JR. Is the 16S–23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol. 2001;18:1057–69.PubMed 

    Google Scholar 
    Fisher MM, Triplett EW. Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol. 1999;65:4630–6.PubMed 
    PubMed Central 

    Google Scholar 
    Brown BL, Watson M, Minot SS, Rivera MC, Franklin RB. MinIONTM nanopore sequencing of environmental metagenomes: a synthetic approach. Gigascience. 2017;6:1–10.PubMed 
    PubMed Central 

    Google Scholar 
    Hernando-Morales V, Varela MM, Needham DM, Cram J, Fuhrman JA, Teira E. Vertical and seasonal patterns control bacterioplankton communities at two horizontally coherent coastal upwelling sites off Galicia (NW Spain). Microb Ecol. 2018;76:866–84.PubMed 

    Google Scholar 
    Johnson JS, Spakowicz DJ, Hong B-Y, Petersen LM, Demkowicz P, Chen L, et al. Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 2019;10:5029.PubMed 
    PubMed Central 

    Google Scholar 
    Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored ‘rare biosphere’. Proc Natl Acad Sci USA. 2006;103:12115–20.PubMed 
    PubMed Central 

    Google Scholar 
    Nossa CW, Oberdorf WE, Yang L, Aas JA, Paster BJ, Desantis TZ, et al. Design of 16S rRNA gene primers for 454 pyrosequencing of the human foregut microbiome. World J Gastroenterol. 2010;16:4135–44.PubMed 
    PubMed Central 

    Google Scholar 
    Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature. 2008;456:53–9.PubMed 
    PubMed Central 

    Google Scholar 
    Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature. 2017;551:457–63.PubMed 
    PubMed Central 

    Google Scholar 
    Kapustina Ž, Medžiūnė J, Alzbutas G, Rokaitis I, Matjošaitis K, Mackevičius G, et al. High-resolution microbiome analysis enabled by linking of 16S rRNA gene sequences with adjacent genomic contexts. Microb Genom. 2021;7:1–16.
    Google Scholar 
    Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, et al. Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature. 2004;428:37–43.PubMed 

    Google Scholar 
    Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science. 2004;304:66–74.PubMed 

    Google Scholar 
    Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 2007;5:e77.PubMed 
    PubMed Central 

    Google Scholar 
    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–7.PubMed 
    PubMed Central 

    Google Scholar 
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.PubMed 
    PubMed Central 

    Google Scholar 
    Karst SM, Ziels RM, Kirkegaard RH, Sørensen EA, McDonald D, Zhu Q, et al. High-accuracy long-read amplicon sequences using unique molecular identifiers with Nanopore or PacBio sequencing. Nat Methods. 2021;18:165–9.PubMed 

    Google Scholar 
    Jamy M, Foster R, Barbera P, Czech L, Kozlov A, Stamatakis A, et al. Long-read metabarcoding of the eukaryotic rDNA operon to phylogenetically and taxonomically resolve environmental diversity. Mol Ecol Resour. 2020;20:429–43.PubMed 

    Google Scholar 
    Leggett RM, Clark MD. A world of opportunities with nanopore sequencing. J Exp Bot. 2017;68:5419–29.PubMed 

    Google Scholar 
    Jain M, Olsen HE, Paten B, Akeson M. The Oxford nanopore MinION: delivery of nanopore sequencing to the genomics community. Genome Biol. 2016;17:239.PubMed 
    PubMed Central 

    Google Scholar 
    Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, et al. Real-time DNA sequencing from single polymerase molecules. Science. 2009;323:133–8.PubMed 

    Google Scholar 
    Graf J, Ledala N, Caimano MJ, Jackson E, Gratalo D, Fasulo D, et al. High-resolution differentiation of enteric bacteria in premature infant fecal microbiomes using a novel rRNA amplicon. mBio. 2021;12:e03656–20.PubMed 
    PubMed Central 

    Google Scholar 
    Martijn J, Lind AE, Schön ME, Spiertz I, Juzokaite L, Bunikis I, et al. Confident phylogenetic identification of uncultured prokaryotes through long read amplicon sequencing of the 16S-ITS-23S rRNA operon. Environ Microbiol. 2019;21:2485–98.PubMed 
    PubMed Central 

    Google Scholar 
    Okazaki Y, Fujinaga S, Salcher MM, Callieri C, Tanaka A, Kohzu A, et al. Microdiversity and phylogeographic diversification of bacterioplankton in pelagic freshwater systems revealed through long-read amplicon sequencing. Microbiome. 2021;9:24.PubMed 
    PubMed Central 

    Google Scholar 
    Miga KH, Koren S, Rhie A, Vollger MR, Gershman A, Bzikadze A, et al. Telomere-to-telomere assembly of a complete human X chromosome. Nature. 2020;585:79–84.PubMed 
    PubMed Central 

    Google Scholar 
    Wenger AM, Peluso P, Rowell WJ, Chang P-C, Hall RJ, Concepcion GT, et al. Accurate circular consensus long-read sequencing improves variant detection and assembly of a human genome. Nat Biotechnol. 2019;37:1155–62.PubMed 
    PubMed Central 

    Google Scholar 
    Matsuo Y, Komiya S, Yasumizu Y, Yasuoka Y, Mizushima K, Takagi T, et al. Full-length 16S rRNA gene amplicon analysis of human gut microbiota using MinIONTM nanopore sequencing confers species-level resolution. BMC Microbiol. 2021;21:35.PubMed 
    PubMed Central 

    Google Scholar 
    Calus ST, Ijaz UZ, Pinto AJ. NanoAmpli-Seq: a workflow for amplicon sequencing for mixed microbial communities on the nanopore sequencing platform. Gigascience. 2018;7:1–16.
    Google Scholar 
    Callahan BJ, Wong J, Heiner C, Oh S, Theriot CM, Gulati AS, et al. High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution. Nucleic Acids Res. 2019;47:e103–e103.PubMed 
    PubMed Central 

    Google Scholar 
    Benítez-Páez A, Portune KJ, Sanz Y. Species-level resolution of 16S rRNA gene amplicons sequenced through the MinIONTM portable nanopore sequencer. Gigascience. 2016;5:4.PubMed 
    PubMed Central 

    Google Scholar 
    Kumar V, Vollbrecht T, Chernyshev M, Mohan S, Hanst B, Bavafa N, et al. Long-read amplicon denoising. Nucleic Acids Res. 2019;47:e104–e104.PubMed 
    PubMed Central 

    Google Scholar 
    Wick RR, Judd LM, Holt KE. Performance of neural network basecalling tools for Oxford Nanopore sequencing. Genome Biol. 2019;20:129.PubMed 
    PubMed Central 

    Google Scholar 
    Lane D. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds). Nucleic acid techniques in bacterial systematics. 1991. Wiley, New York, pp 115–75.Miller CS, Handley KM, Wrighton KC, Frischkorn KR, Thomas BC, Banfield JF. Short-read assembly of full-length 16S amplicons reveals bacterial diversity in subsurface sediments. PLoS One. 2013;8:e56018–e56018.PubMed 
    PubMed Central 

    Google Scholar 
    Hunt DE, Klepac-Ceraj V, Acinas SG, Gautier C, Bertilsson S, Polz MF. Evaluation of 23S rRNA PCR primers for use in phylogenetic studies of bacterial diversity. Appl Environ Microbiol. 2006;72:2221–5.PubMed 
    PubMed Central 

    Google Scholar 
    Volden R, Palmer T, Byrne A, Cole C, Schmitz RJ, Green RE, et al. Improving nanopore read accuracy with the R2C2 method enables the sequencing of highly multiplexed full-length single-cell cDNA. Proc Natl Acad Sci. 2018;115:9726 LP–9731.
    Google Scholar 
    Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods. 2009;6:343–5.PubMed 

    Google Scholar 
    Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.PubMed 
    PubMed Central 

    Google Scholar 
    Eddy SR. A new generation of homology search tools based on probabilistic inference. Genome Inform. 2009;23:205–11.PubMed 

    Google Scholar 
    Morisse P, Marchet C, Limasset A, Lecroq T, Lefebvre A. Scalable long read self-correction and assembly polishing with multiple sequence alignment. Sci Rep. 2021;11:761.PubMed 
    PubMed Central 

    Google Scholar 
    Do CB, Mahabhashyam MSP, Brudno M, Batzoglou S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res. 2005;15:330–40.PubMed 
    PubMed Central 

    Google Scholar 
    dos Santos HRM, Argolo CS, Argôlo-Filho RC, Loguercio LL. A 16S rDNA PCR-based theoretical to actual delta approach on culturable mock communities revealed severe losses of diversity information. BMC Microbiol. 2019;19:74.PubMed 
    PubMed Central 

    Google Scholar 
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.PubMed 

    Google Scholar 
    Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28:3150–2.PubMed 
    PubMed Central 

    Google Scholar 
    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.PubMed 
    PubMed Central 

    Google Scholar 
    Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3.PubMed 
    PubMed Central 

    Google Scholar 
    Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–W259.PubMed 
    PubMed Central 

    Google Scholar 
    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112 LP–5120.
    Google Scholar 
    Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42:D633–42.PubMed 

    Google Scholar 
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596.PubMed 

    Google Scholar 
    de Oliveira Martins L, Page AJ, Mather AE, Charles IG. Taxonomic resolution of the ribosomal RNA operon in bacteria: implications for its use with long-read sequencing. NAR Genom Bioinform. 2019;2:lqz016–lqz016.PubMed 
    PubMed Central 

    Google Scholar 
    Olesen SW, Duvallet C, Alm EJ. dbOTU3: a new implementation of distribution-based OTU calling. PLoS One. 2017;12:e0176335–e0176335.PubMed 
    PubMed Central 

    Google Scholar 
    Fichot EB, Norman RS. Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform. Microbiome. 2013;1:10.PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Mito-nuclear selection induces a trade-off between species ecological dominance and evolutionary lifespan

    Hagen, O. et al. gen3sis: a general engine for eco-evolutionary simulations of the processes that shape Earth’s biodiversity. PLoS Biol. 19, e3001340 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Urban, M. C. et al. Evolutionary origins for ecological patterns in space. Proc. Natl Acad. Sci. USA 117, 17482–17490 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (MPB-32) (Princeton Univ. Press, 2001).Volkov, I., Banavar, J. R., Hubbell, S. P. & Maritan, A. Neutral theory and relative species abundance in ecology. Nature 424, 1035–1037 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    McGill, B. J. et al. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett. 10, 995–1015 (2007).PubMed 
    Article 

    Google Scholar 
    de Aguiar, M. A. M., Baranger, M., Baptestini, E. M., Kaufman, L. & Bar-Yam, Y. Global patterns of speciation and diversity. Nature 460, 384 (2009).PubMed 
    Article 

    Google Scholar 
    O’Dwyer, J. P. & Green, J. L. Field theory for biogeography: a spatially explicit model for predicting patterns of biodiversity. Ecol. Lett. 13, 87–95 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Chisholm, R. A. & Pacala, S. W. Niche and neutral models predict asymptotically equivalent species abundance distributions in high-diversity ecological communities. Proc. Natl Acad. Sci. USA 107, 15821–15825 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Mutshinda, C. M., O’Hara, R. B. & Woiwod, I. P. What drives community dynamics? Proc. R. Soc. B 276, 2923–2929 (2009).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rosindell, J., Cornell, S. J., Hubbell, S. P. & Etienne, R. S. Protracted speciation revitalizes the neutral theory of biodiversity. Ecol. Lett. 13, 716–727 (2010).PubMed 
    Article 

    Google Scholar 
    Chisholm, R. A. & O’Dwyer, J. P. Species ages in neutral biodiversity models. Theor. Popul. Biol. 93, 85–94 (2014).PubMed 
    Article 

    Google Scholar 
    Nee, S. The neutral theory of biodiversity: do the numbers add up? Funct. Ecol. 19, 173–176 (2005).Article 

    Google Scholar 
    Ricklefs, R. E. A comment on Hubbell’s zero-sum ecological drift model. Oikos 100, 185–192 (2003).Article 

    Google Scholar 
    Etienne, R. S., Apol, M. E. F., Olff, H. & Weissing, F. J. Modes of speciation and the neutral theory of biodiversity. Oikos 116, 241–258 (2007).Article 

    Google Scholar 
    Davies, T. J., Allen, A. P., Borda-de Água, L., Regetz, J. & Melián, C. J. Neutral biodiversity theory can explain the imbalance of phylogenetic trees but not the tempo of their diversification. Evolution 65, 1841–1850 (2011).PubMed 
    Article 

    Google Scholar 
    Higgs, P. G. & Derrida, B. Stochastic models for species formation in evolving populations. J. Phys. A 24, L985 (1991).Article 

    Google Scholar 
    Gavrilets, S., Li, H. & Vose, M. D. Rapid parapatric speciation on holey adaptive landscapes. Proc. R. Soc. B 265, 1483–1489 (1998).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Dieckmann, U. & Doebeli, M. On the origin of species by sympatric speciation. Nature 400, 354 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gavrilets, S. & Vose, A. Dynamic patterns of adaptive radiation. Proc. Natl Acad. Sci. USA 102, 18040–18045 (2005).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nosil, P. Ecological Speciation (Oxford Univ. Press, 2012).Gavrilets, S., Acton, R. & Gravner, J. Dynamics of speciation and diversification in a metapopulation. Evolution 54, 1493–1501 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Costa, C. L. N. et al. Signatures of microevolutionary processes in phylogenetic patterns. Syst. Biol. 68, 131–144 (2018).
    Google Scholar 
    Li, J., Huang, J.-P., Sukumaran, J. & Knowles, L. L. Microevolutionary processes impact macroevolutionary patterns. BMC Evol. Biol. 18, 123 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Melián, C. J., Alonso, D., Allesina, S., Condit, R. S. & Etienne, R. S. Does sex speed up evolutionary rate and increase biodiversity? PLoS Comput. Biol. 8, e1002414 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rangel, T. F. et al. Modeling the ecology and evolution of biodiversity: biogeographical cradles, museums, and graves. Science 361, eaar5452 (2018).Pontarp, M. et al. The latitudinal diversity gradient: novel understanding through mechanistic eco-evolutionary models. Trends Ecol. Evol. 34, 211–223 (2019).PubMed 
    Article 

    Google Scholar 
    de Alencar, L. R. V. & Quental, T. B. Linking population-level and microevolutionary processes to understand speciation dynamics at the macroevolutionary scale. Ecol. Evol. 11, 5828–5843 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hurlbert, A. H. & Stegen, J. C. When should species richness be energy limited, and how would we know? Ecol. Lett. 17, 401–413 (2014).PubMed 
    Article 

    Google Scholar 
    Morlon, H. Phylogenetic approaches for studying diversification. Ecol. Lett. 17, 508–525 (2014).PubMed 
    Article 

    Google Scholar 
    Rosindell, J., Harmon, L. J. & Etienne, R. S. Unifying ecology and macroevolution with individual-based theory. Ecol. Lett. 18, 472–482 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rosindell, J. & Harmon, L. J. A unified model of species immigration, extinction and abundance on islands. J. Biogeogr. 40, 1107–1118 (2013).Article 

    Google Scholar 
    Etienne, R. S. & Rosindell, J. Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification. Syst. Biol. 61, 204–213 (2012).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rabosky, D. L. & Matute, D. R. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. Proc. Natl Acad. Sci. USA 110, 15354–15359 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Louca, S. & Pennell, M. W. Extant timetrees are consistent with a myriad of diversification histories. Nature 580, 502–505 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Princepe, D. & De Aguiar, M. A. M. Modeling mito-nuclear compatibility and its role in species identification. Syst. Biol. 70, 133–144 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Bar-Yaacov, D., Blumberg, A. & Mishmar, D. Mitochondrial-nuclear co-evolution and its effects on OXPHOS activity and regulation. Biochim. Biophys. Acta 1819, 1107–1111 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    Sunnucks, P., Morales, H. E., Lamb, A. M., Pavlova, A. & Greening, C. Integrative approaches for studying mitochondrial and nuclear genome co-evolution in oxidative phosphorylation. Front. Genet. 8, 25 (2017).PubMed 
    PubMed Central 
    Article 

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

    Google Scholar 
    Lima, T. G., Burton, R. S. & Willett, C. S. Genomic scans reveal multiple mito-nuclear incompatibilities in population crosses of the copepod Tigriopus californicus. Evolution 73, 609–620 (2019).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 https://doi.org/10.1098/rspb.2013.1521 (2013).Hill, G. E. Mitonuclear compensatory coevolution. Trends Genet. 36, 403–414 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Gershoni, M., Templeton, A. R. & Mishmar, D. Mitochondrial bioenergetics as a major motive force of speciation. BioEssays 31, 642–650 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hill, G. E. Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap. Ecol. Evol. 6, 5831–5842 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tobler, M., Barts, N. & Greenway, R. Mitochondria and the origin of species: bridging genetic and ecological perspectives on speciation processes. Integr. Comp. Biol. 59, 900–911 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    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 
    Telschow, A., Gadau, J., Werren, J. H. & Kobayashi, Y. Genetic incompatibilities between mitochondria and nuclear genes: effect on gene flow and speciation. Front. Genet. 10, 62 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lane, N. Biodiversity: on the origin of bar codes. Nature 462, 272–274 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hill, G. E Mitonuclear Ecology (Oxford Univ. Press, 2019).Wolff, J. N., Ladoukakis, E. D., Enríquez, J. A. & Dowling, D. K. Mitonuclear interactions: evolutionary consequences over multiple biological scales. Philos. Trans. R. Soc. B 369, 20130443 (2014).Article 

    Google Scholar 
    Koch, R. E. et al. Integrating mitochondrial aerobic metabolism into ecology and evolution. Trends Ecol. Evol. 36, 321–332 (2021).PubMed 
    Article 

    Google Scholar 
    Weir, J. T. & Schluter, D. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315, 1574–1576 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Botero, C. A., Dor, R., McCain, C. M. & Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Mol. Ecol. 23, 259–268 (2014).PubMed 
    Article 

    Google Scholar 
    Weir, J. T. Environmental harshness, latitude and incipient speciation. Mol. Ecol. 23, 251–253 (2014).PubMed 
    Article 

    Google Scholar 
    Schluter, D. & Pennell, M. W. Speciation gradients and the distribution of biodiversity. Nature 546, 48–55 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Harvey, M. G. et al. The evolution of a tropical biodiversity hotspot. Science 370, 1343–1348 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rabosky, D. L. et al. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559, 392–395 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rabosky, D. L. & Hurlbert, A. H. Species richness at continental scales is dominated by ecological limits. Am. Nat. 185, 572–583 (2015).PubMed 
    Article 

    Google Scholar 
    Sugihara, G. Minimal community structure: an explanation of species abundance patterns. Am. Nat. 116, 770–787 (1980).PubMed 
    Article 

    Google Scholar 
    Zhang, F. & Broughton, R. E. Mitochondrial–nuclear interactions: compensatory evolution or variable functional constraint among vertebrate oxidative phosphorylation genes? Genome Biol. Evol. 5, 1781–1791 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Piccinini, G. et al. Mitonuclear coevolution, but not nuclear compensation, drives evolution of OXPHOS complexes in bivalves. Mol. Biol. Evol. 38, 2597–2614 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Barreto, F. S. et al. Genomic signatures of mitonuclear coevolution across populations of Tigriopus californicus. Nat. Ecol. Evol. 2, 1250–1257 (2018).PubMed 
    Article 

    Google Scholar 
    Kennedy, J. D. et al. Into and out of the tropics: the generation of the latitudinal gradient among New World passerine birds. J. Biogeogr. 41, 1746–1757 (2014).Article 

    Google Scholar 
    Etienne, R. S. et al. A minimal model for the latitudinal diversity gradient suggests a dominant role for ecological limits. Am. Nat. 194, E122–E133 (2019).PubMed 
    Article 

    Google Scholar 
    Mittelbach, G. G. et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10, 315–331 (2007).PubMed 
    Article 

    Google Scholar 
    Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192–211 (2004).PubMed 
    Article 

    Google Scholar 
    Evans, K. L. & Gaston, K. J. Can the evolutionary-rates hypothesis explain species–energy relationships? Funct. Ecol. 19, 899–915 (2005).Article 

    Google Scholar 
    Allen, A. P. & Gillooly, J. F. Assessing latitudinal gradients in speciation rates and biodiversity at the global scale. Ecol. Lett. 9, 947–954 (2006).PubMed 
    Article 

    Google Scholar 
    Cutter, A. D. & Gray, J. C. Ephemeral ecological speciation and the latitudinal biodiversity gradient. Evolution 70, 2171–2185 (2016).PubMed 
    Article 

    Google Scholar 
    Dowling, D. K., Abiega, K. C. & Arnqvist, G. Temperature-specific outcomes of cytoplasmic–nuclear interactions on egg-to-adult development time in seed beetles. Evolution 61, 194–201 (2007).PubMed 
    Article 

    Google Scholar 
    Smith, B. T., Seeholzer, G. F., Harvey, M. G., Cuervo, A. M. & Brumfield, R. T. A latitudinal phylogeographic diversity gradient in birds. PLoS Biol. 15, e2001073 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Freeman, B. G., Weeks, T., Schluter, D. & Tobias, J. A. The latitudinal gradient in rates of evolution for bird beaks, a species interaction trait. Ecol. Lett. 25, 635–646 (2022).PubMed 
    Article 

    Google Scholar 
    Vellend, M. Species diversity and genetic diversity: parallel processes and correlated patterns. Am. Nat. 166, 199–215 (2005).PubMed 
    Article 

    Google Scholar 
    Pontarp, M. & Wiens, J. J. The origin of species richness patterns along environmental gradients: uniting explanations based on time, diversification rate and carrying capacity. J. Biogeogr. 44, 722–735 (2017).Article 

    Google Scholar 
    Harvey, M. G. et al. Positive association between population genetic differentiation and speciation rates in New World birds. Proc. Natl Acad. Sci. USA 114, 6328–6333 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Araújo, M. S. & Costa-Pereira, R. Latitudinal gradients in intraspecific ecological diversity. Biol. Lett. 9, 20130778 (2013).Derrida, B. & Peliti, L. Evolution in a flat fitness landscape. Bull. Math. Biol. 53, 355–382 (1991).Article 

    Google Scholar 
    de Aguiar, M. A. M. Speciation in the Derrida–Higgs model with finite genomes and spatial populations. J. Phys. A 50, 85602 (2017).Article 

    Google Scholar 
    Thibert-Plante, X. & Gavrilets, S. Evolution of mate choice and the so-called magic traits in ecological speciation. Ecol. Lett. 16, 1004–1013 (2013).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).PubMed 
    Article 

    Google Scholar 
    Kearns, A. M. et al. Genomic evidence of speciation reversal in ravens. Nat. Commun. 9, 906 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Gray, J. S., Bjørgesæter, A. & Ugland, K. I. On plotting species abundance distributions. J. Anim. Ecol. 75, 752–756 (2006).PubMed 
    Article 

    Google Scholar  More

  • in

    Warming reduces global agricultural production by decreasing cropping frequency and yields

    Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).CAS 
    Article 

    Google Scholar 
    Mueller, N. D. et al. Closing yield gaps through nutrient and water management. Nature 490, 254–257 (2012).CAS 
    Article 

    Google Scholar 
    Hong, C. et al. Global and regional drivers of land-use emissions in 1961–2017. Nature 589, 554–561 (2021).CAS 
    Article 

    Google Scholar 
    Laurance, W. F., Sayer, J. & Cassman, K. G. Agricultural expansion and its impacts on tropical nature. Trends Ecol. Evol. 29, 107–116 (2014).Article 

    Google Scholar 
    Cassman, K. G. & Grassini, P. A global perspective on sustainable intensification research. Nat. Sustain. 3, 262–268 (2020).Article 

    Google Scholar 
    Hodge, I., Hauck, J. & Bonn, A. The alignment of agricultural and nature conservation policies in the European Union. Conserv. Biol. 29, 996–1005 (2015).Article 

    Google Scholar 
    Heilmayr, R., Rausch, L. L., Munger, J. & Gibbs, H. K. Brazil’s Amazon Soy Moratorium reduced deforestation. Nat. Food 1, 801–810 (2020).Article 

    Google Scholar 
    Diffenbaugh, N. S. et al. Quantifying the influence of global warming on unprecedented extreme climate events. Proc. Natl Acad. Sci. USA 114, 4881–4886 (2017).CAS 
    Article 

    Google Scholar 
    Iizumi, T. & Ramankutty, N. How do weather and climate influence cropping area and intensity? Glob. Food Security 4, 46–50 (2015).Article 

    Google Scholar 
    Davis, K. F., Downs, S. & Gephart, J. A. Towards food supply chain resilience to environmental shocks. Nat. Food 2, 54–65 (2020).Article 

    Google Scholar 
    Wang, X. et al. Emergent constraint on crop yield response to warmer temperature from field experiments. Nat. Sustain. 3, 908–916 (2020).Article 

    Google Scholar 
    Lobell, D. B., Schlenker, W. & Costa-Roberts, J. Climate trends and global crop production since 1980. Science 333, 616–620 (2011).CAS 
    Article 

    Google Scholar 
    Sloat, L. L. et al. Climate adaptation by crop migration. Nat. Commun. 11, 1243 (2020).CAS 
    Article 

    Google Scholar 
    Afifi, T., Liwenga, E. & Kwezi, L. Rainfall-induced crop failure, food insecurity and out-migration in Same-Kilimanjaro, Tanzania. Clim. Dev. 6, 53–60 (2014).Article 

    Google Scholar 
    Stigter, K. in Applied Agrometeorology (ed. Stigter, K.) 531–534 (Springer, 2010).Seifert, C. A. & Lobell, D. B. Response of double cropping suitability to climate change in the United States. Environ. Res. Lett. 10, 024002 (2015).Article 

    Google Scholar 
    Kawasaki, K. Two harvests are better than one: double cropping as a strategy for climate change adaptation. Am. J. Agr. Econ. 101, 172–192 (2019).Article 

    Google Scholar 
    Ceglar, A., Zampieri, M., Toreti, A. & Dentener, F. Observed northward migration of agro‐climate zones in Europe will further accelerate under climate change. Earths Future 7, 1088–1101 (2019).Article 

    Google Scholar 
    Cohn, A. S., VanWey, L. K., Spera, S. A. & Mustard, J. F. Cropping frequency and area response to climate variability can exceed yield response. Nat. Clim. Change 6, 601–604 (2016).Article 

    Google Scholar 
    Challinor, A. J., Simelton, E. S., Fraser, E. D. G., Hemming, D. & Collins, M. Increased crop failure due to climate change: assessing adaptation options using models and socio-economic data for wheat in China. Environ. Res. Lett. 5, 034012 (2010).Article 

    Google Scholar 
    Ray, D. K. & Foley, J. A. Increasing global crop harvest frequency: recent trends and future directions. Environ. Res. Lett. 8, 044041 (2013).Article 

    Google Scholar 
    Wu, W. et al. Global cropping intensity gaps: increasing food production without cropland expansion. Land Use Policy 76, 515–525 (2018).Article 

    Google Scholar 
    Pugh, T. A. M. et al. Climate analogues suggest limited potential for intensification of production on current croplands under climate change. Nat. Commun. 7, 12608 (2016).CAS 
    Article 

    Google Scholar 
    Scherer, L. A., Verburg, P. H. & Schulp, C. J. E. Opportunities for sustainable intensification in European agriculture. Glob. Environ. Change 48, 43–55 (2018).Article 

    Google Scholar 
    Qin, Y. et al. Agricultural risks from changing snowmelt. Nat. Clim. Change 10, 459–465 (2020).Article 

    Google Scholar 
    Waha, K. et al. Multiple cropping systems of the world and the potential for increasing cropping intensity. Glob. Environ. Change 64, 102131 (2020).Article 

    Google Scholar 
    Raderschall, C. A., Vico, G., Lundin, O., Taylor, A. R. & Bommarco, R. Water stress and insect herbivory interactively reduce crop yield while the insect pollination benefit is conserved. Glob. Chang. Biol. 27, 71–83 (2021).CAS 
    Article 

    Google Scholar 
    Ding, M. et al. Variation in cropping intensity in Northern China from 1982 to 2012 based on GIMMS-NDVI data. Sustainability 8, 1123 (2016).Article 

    Google Scholar 
    Yu, Q., Xiang, M., Sun, Z. & Wu, W. The complexity of measuring cropland use intensity: an empirical study. Agr. Syst. 192, 103180 (2021).Article 

    Google Scholar 
    Moore, F. C. & Lobell, D. B. Adaptation potential of European agriculture in response to climate change. Nat. Clim. Change 4, 610–614 (2014).Article 

    Google Scholar 
    Agnolucci, P. et al. Impacts of rising temperatures and farm management practices on global yields of 18 crops. Nat. Food 1, 562–571 (2020).Article 

    Google Scholar 
    Zhu, P. & Burney, J. Temperature‐driven harvest decisions amplify US winter wheat loss under climate warming. Glob. Change Biol. 27, 550–562 (2021).CAS 
    Article 

    Google Scholar 
    Ortiz-Bobea, A., Knippenberg, E. & Chambers, R. G. Growing climatic sensitivity of U.S. agriculture linked to technological change and regional specialization. Sci. Adv. 4, 4343 (2018).Article 

    Google Scholar 
    Duku, C., Zwart, S. J. & Hein, L. Impacts of climate change on cropping patterns in a tropical, sub-humid watershed. PLoS ONE 13, 0192642 (2018).Article 

    Google Scholar 
    Folberth, C. et al. The global cropland-sparing potential of high-yield farming. Nat. Sustain. 3, 281–289 (2020).Article 

    Google Scholar 
    Lobell, D. B. et al. The critical role of extreme heat for maize production in the United States. Nat. Clim. Change 3, 497–501 (2013).Article 

    Google Scholar 
    Yang, X. et al. Potential benefits of climate change for crop productivity in China. Agric. For. Meteorol. 208, 76–84 (2015).Article 

    Google Scholar 
    Burney, J., Woltering, L. & Burke, M. Solar-powered drip irrigation enhances food security in the Sudano–Sahel. Proc. Natl Acad. Sci. USA 107, 1848–1853 (2010).CAS 
    Article 

    Google Scholar 
    You, L. et al. What is the irrigation potential for Africa? A combined biophysical and socioeconomic approach. Food Policy 36, 770–782 (2011).Article 

    Google Scholar 
    Zheng, B., Chenu, K., Fernanda Dreccer, M. & Chapman, S. C. Breeding for the future: what are the potential impacts of future frost and heat events on sowing and flowering time requirements for Australian bread wheat (Triticum aestivium) varieties? Glob. Change Biol. 18, 2899–2914 (2012).Article 

    Google Scholar 
    Flach, R., Fader, M., Folberth, C., Skalský, R. & Jantke, K. The effects of cropping intensity and cropland expansion of Brazilian soybean production on green water flows. Environ. Res. Commun. 2, 071001 (2020).Article 

    Google Scholar 
    Wood, S. A., Jina, A. S., Jain, M., Kristjanson, P. & DeFries, R. S. Smallholder farmer cropping decisions related to climate variability across multiple regions. Glob. Environ. Change 25, 163–172 (2014).Article 

    Google Scholar 
    Paola, A. D. et al. The expansion of wheat thermal suitability of Russia in response to climate change. Land Use Policy 78, 70–77 (2018).Article 

    Google Scholar 
    Brunelle, T. & Makowski, D. Assessing whether the best land is cultivated first: a quantile analysis. PLoS ONE 15, e0242222 (2020).CAS 
    Article 

    Google Scholar 
    Lark, T. J., Spawn, S. A., Bougie, M. & Gibbs, H. K. Cropland expansion in the United States produces marginal yields at high costs to wildlife. Nat. Commun. 11, 4295 (2020).CAS 
    Article 

    Google Scholar 
    Zabel, F., Putzenlechner, B. & Mauser, W. Global agricultural land resources—a high resolution suitability evaluation and its perspectives until 2100 under climate change conditions. PLoS ONE 9, e107522 (2014).Article 

    Google Scholar 
    Petkeviciene, B. The effects of climate factors on sugar beet early sowing timing. Agron. Res. 7, 436–443 (2009).
    Google Scholar 
    Ainsworth, E. A. & Long, S. P. 30 years of free-air carbon dioxide enrichment (FACE): what have we learned about future crop productivity and its potential for adaptation? Glob. Change Biol. 27, 27–49 (2021).CAS 
    Article 

    Google Scholar 
    Collins, M. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) Ch. 11 (Cambridge Univ. Press, 2013).Pendergrass, A. G., Knutti, R., Lehner, F., Deser, C. & Sanderson, B. M. Precipitation variability increases in a warmer climate. Sci. Rep. 7, 17966 (2017).Article 

    Google Scholar 
    Asadieh, B. & Krakauer, N. Y. Global trends in extreme precipitation: climate models versus observations. Hydrol. Earth Syst. Sci. 19, 877–891 (2015).Article 

    Google Scholar 
    Zhang, Y., You, L., Lee, D. & Block, P. Integrating climate prediction and regionalization into an agro-economic model to guide agricultural planning. Clim. Change 158, 435–451 (2020).Article 

    Google Scholar 
    Turner, S. W. D., Hejazi, M., Yonkofski, C., Kim, S. H. & Kyle, P. Influence of groundwater extraction costs and resource depletion limits on simulated global nonrenewable water withdrawals over the twenty‐first century. Earths Future 7, 123–135 (2019).Article 

    Google Scholar 
    Zhu, W., Jia, S., Devineni, N., Lv, A. & Lall, U. Evaluating China’s water security for food production: the role of rainfall and irrigation. Geophys. Res. Lett. 46, 11155–11166 (2019).Article 

    Google Scholar 
    FAOSTAT (Food and Agriculture Organization of the United Nations, 1997).Egli, L., Schröter, M., Scherber, C., Tscharntke, T. & Seppelt, R. Crop asynchrony stabilizes food production. Nature 588, E7–E12 (2020).CAS 
    Article 

    Google Scholar 
    Hersbach, H. et al. ERA5 Hourly Data on Single Levels from 1979 to Present (Copernicus Climate Change Service (C3S) Climate Data Store (CDS), accessed 1 August 2020); https://doi.org/10.24381/cds.adbb2d47 (2018).Feng, P. et al. Impacts of rainfall extremes on wheat yield in semi-arid cropping systems in eastern Australia. Clim. Change 147, 555–569 (2018).Article 

    Google Scholar 
    Teluguntla, P. et al. in Land Resources Monitoring, Modeling, and Mapping with Remote Sensing (ed. Thenkabail, P. S.) 849 (CRC Press, 2015).Hawkins, E. et al. Increasing influence of heat stress on French maize yields from the 1960s to the 2030s. Glob. Change Biol. 19, 937–947 (2013).Article 

    Google Scholar 
    Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).Article 

    Google Scholar 
    Lobell, D. B., Bänziger, M., Magorokosho, C. & Vivek, B. Nonlinear heat effects on African maize as evidenced by historical yield trials. Nat. Clim. Change 1, 42–45 (2011).Article 

    Google Scholar 
    Deryng, D., Sacks, W. J., Barford, C. C. & Ramankutty, N. Simulating the effects of climate and agricultural management practices on global crop yield. Glob. Biogeochem. Cycles 25, GB2006 (2011).New, M., New, M., Lister, D., Hulme, M. & Makin, I. A high-resolution data set of surface climate over global land areas. Clim. Res. 21, 1–25 (2002).Article 

    Google Scholar 
    Willmott, C. J. Terrestrial Air Temperature and Precipitation: Monthly and Annual Time Series (1950–1996) (Center for Climatic Research, 2000); http://climate.geog.udel.edu/~climate/html_pages/README.ghcn_ts2.htmlVan Beveren, I. Total factor productivity estimation: a practical review. J. Econ. Surv. 26, 98–128 (2012).Article 

    Google Scholar 
    Xu, J. et al. Double cropping and cropland expansion boost grain production in Brazil. Nat. Food 2, 264–273 (2021).Article 

    Google Scholar 
    Friedl, M. & Gray, J. MCD12Q2 MODIS/Terra+ Aqua Land Cover Dynamics Yearly L3 Global 500 m SIN Grid V006 (NASA EOSDIS, 2019).Sulla-Menashe, D. & Friedl, M. A. User Guide to Collection 6 MODIS Land Cover (MCD12Q1 and MCD12C1) Product (USGS, 2018).Schwalm, C. R., Glendon, S. & Duffy, P. B. RCP8.5 tracks cumulative CO2 emissions. Proc. Natl Acad. Sci. USA 117, 19656–19657 (2020).CAS 
    Article 

    Google Scholar 
    Lange, S. Trend-preserving bias adjustment and statistical downscaling with ISIMIP3BASD (v1.0). Geosci. Model Dev. 12, 3055–3070 (2019).Article 

    Google Scholar 
    Peng Zhu. Climate effects on caloric yield and cropping frequency. Zenodo https://doi.org/10.5281/zenodo.7038556 (2022). More

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    Author Correction: Widespread extinction debts and colonization credits in United States breeding bird communities

    In the version of this article initially published, there were errors in equations and notations in the Methods “Model development” subsection which arose during manuscript preparation; the errors affect presentation of the study but not the analysis, results, or code provided with the article. Clarifications to text and equations follow.In Equation (1), “N” replaces “Normal”; in Equations (2), (3), (7) and in text directly below Equations (3), (5) and (7), “ys,i,z” now replaces “Δxs,t1, t2.” In the two paragraphs below Equation (2), “t2 = 2016” and “t1 = 2001” now replace “2016” and “2001” in five instances. Further, Equations (5)–(7) have been revised as follows:$$begin{array}{ll}fleft( {x_{s,t}} right) = {{{mathrm{exp}}}} & left( {beta _0 + mathop {sum }limits_{i = 1}^{I = 5} beta _{1,i} x_{s,i,t} + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = i}^{K = 5} beta _{2,i,k}x_{s,i,t}x_{k,s,t}}right. \ & quad quad left. {+ mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = 1, k neq i}^{K = 5} beta _{3,i,k}x_{s,i,t}x_{k,s,t}} right)end{array} {rm{Revised}} {rm{Eq}}. (5)$$$$begin{array}{ll}fleft( {x_{s,t}} right) \ = expleft( {beta _0 + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{j = 1}^{J = 2} beta _{0,i,j,}x_{i,s,t}^j + mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{k = i + 1}^{K = 6} beta _{1,i,k}x_{i,s,t}x_{k,s,t}} right) {mathrm{Original}} {rm{Eq}}. (5)end{array}$$$$y_{s,i,z} = left{ {begin{array}{*{20}{l}} {y_{s,i,1} = left| {Delta x_{s,i}} right|,} hfill & {y_{s,i,2} = 0,} hfill & {{{{mathrm{if}}}},Delta x_{s,i} < 0} hfill \ {y_{s,i,1} = 0,} hfill & {y_{s,i,2} = Delta x_{s,i}} hfill & {{{{mathrm{otherwise}}}}} hfill end{array}} right. {rm{Revised}} {rm{Eq}}. (6)$$$$x_{i,s,} = left{ {begin{array}{*{20}{l}} {x_{1,i,s} = left| {Delta x_{i,s}} right|,} hfill & {x_{2,i,s} = 0,} hfill & {if,Delta x_{i,s} < 0} hfill \ {x_{1,i,s} = 0,} hfill & {x_{2,i,s} = Delta x_{i,s},} hfill & {otherwise} hfill end{array}} right. {rm{Original}} {rm{Eq}}. (6)$$$$omega left( {y_{s,i,z};gamma } right) = {{{mathrm{exp}}}}left( {mathop {sum }limits_{i = 1}^{I = 5} mathop {sum }limits_{z = 1}^{Z = 2} - gamma _{i,z} y_{s,i,z}} right) {rm{Revised}} {rm{Eq}}. (7)$$$$omega left( {Delta x_{s,t_1,t_2};gamma } right) = expleft( {mathop {sum }limits_{i = 1}^{I = 5} - gamma _{i,z}Delta x_{z,s,i}} right) {rm{Original}} {rm{Eq}}. (7)$$All changes have been made in the HTML and PDF versions of the article. More

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    Plankton response to global warming is characterized by non-uniform shifts in assemblage composition since the last ice age

    Brett, C. E. Sequence stratigraphy, paleoecology, and evolution: biotic clues and responses to sea-level fluctuations. Palaios 13, 241–262 (1998).Article 

    Google Scholar 
    Brett, C. E., Hendy, A. J. W., Bartholomew, A. J., Bonelli, J. R. & McLaughlin, P. I. Response of shallow marine biotas to sea-level fluctuations: a review of faunal replacement and the process of habitat tracking. Palaios 22, 228–244 (2007).Article 

    Google Scholar 
    Parmesan, C. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37, 637–669 (2006).Article 

    Google Scholar 
    Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    Walther, G.-R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Lenoir, J. et al. Species better track climate warming in the oceans than on land. Nat. Ecol. Evol. 4, 1044–1059 (2020).PubMed 
    Article 

    Google Scholar 
    Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).Article 

    Google Scholar 
    Rillo, M. C., Woolley, S. & Hillebrand, H. Drivers of global pre‐industrial patterns of species turnover in planktonic foraminifera. Ecography 2022, e05892 (2021).Article 

    Google Scholar 
    Van der Putten, W. H., Macel, M. & Visser, M. E. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Phil. Trans. R. Soc. B 365, 2025–2034 (2010).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Antão, L. H. et al. Temperature-related biodiversity change across temperate marine and terrestrial systems. Nat. Ecol. Evol. 4, 927–933 (2020).PubMed 
    Article 

    Google Scholar 
    Chen, I. C. et al. Asymmetric boundary shifts of tropical montane Lepidoptera over four decades of climate warming. Glob. Ecol. Biogeogr. 20, 34–45 (2011).Article 

    Google Scholar 
    García Molinos, J. et al. Climate velocity and the future global redistribution of marine biodiversity. Nat. Clim. Change 6, 83–88 (2015).Article 

    Google Scholar 
    Beaugrand, G., Edwards, M., Raybaud, V., Goberville, E. & Kirby, R. R. Future vulnerability of marine biodiversity compared with contemporary and past changes. Nat. Clim. Change 5, 695–701 (2015).Article 

    Google Scholar 
    Benedetti, F. et al. Major restructuring of marine plankton assemblages under global warming. Nat. Commun. 12, 5226 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Occhipinti-Ambrogi, A. Global change and marine communities: alien species and climate change. Mar. Pollut. Bull. 55, 342–352 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    Williams, J. W. & Jackson, S. T. Novel climates, no-analog communities, and ecological surprises. Front. Ecol. Environ. 5, 475–482 (2007).Article 

    Google Scholar 
    Burrows, M. T. et al. Ocean community warming responses explained by thermal affinities and temperature gradients. Nat. Clim. Change 9, 959–963 (2019).Article 

    Google Scholar 
    Dornelas, M. et al. BioTIME: a database of biodiversity time series for the Anthropocene. Glob. Ecol. Biogeogr. 27, 760–786 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jonkers, L. et al. Integrating palaeoclimate time series with rich metadata for uncertainty modelling: strategy and documentation of the PalMod 130k marine palaeoclimate data synthesis. Earth Syst. Sci. Data 12, 1053–1081 (2020).Article 

    Google Scholar 
    Buitenhuis, E. T. et al. MAREDAT: towards a world atlas of MARine Ecosystem DATa. Earth Syst. Sci. Data 5, 227–239 (2013).Article 

    Google Scholar 
    Yasuhara, M., Tittensor, D. P., Hillebrand, H. & Worm, B. Combining marine macroecology and palaeoecology in understanding biodiversity: microfossils as a model. Biol. Rev. 92, 199–215 (2017).PubMed 
    Article 

    Google Scholar 
    Aze, T. et al. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biol. Rev. 86, 900–927 (2011).PubMed 
    Article 

    Google Scholar 
    Takagi, H. et al. Characterizing photosymbiosis in modern planktonic foraminifera. Biogeosciences 16, 3377–3396 (2019).CAS 
    Article 

    Google Scholar 
    Schiebel, R. & Hemleben, C. Planktic Foraminifers in the Modern Ocean (Springer, 2017).Morey, A. E., Mix, A. C. & Pisias, N. G. Planktonic foraminiferal assemblages preserved in surface sediments correspond to multiple environment variables. Quat. Sci. Rev. 24, 925–950 (2005).Article 

    Google Scholar 
    Fenton, I. S., Pearson, P. N., Dunkley Jones, T. & Purvis, A. Environmental predictors of diversity in recent planktonic foraminifera as recorded in marine sediments. PLoS ONE 11, e0165522 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rutherford, S., D’Hondt, S. & Prell, W. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400, 749–753 (1999).CAS 
    Article 

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

    Google Scholar 
    Yasuhara, M., Hunt, G., Dowsett, H. J., Robinson, M. M. & Stoll, D. K. Latitudinal species diversity gradient of marine zooplankton for the last three million years. Ecol. Lett. 15, 1174–1179 (2012).PubMed 
    Article 

    Google Scholar 
    Yasuhara, M. et al. Past and future decline of tropical pelagic biodiversity. Proc. Natl Acad. Sci. USA 117, 12891–12896 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    Beaugrand, G., Reid, P. C., Ibañez, F., Lindley, J. A. & Edwards, M. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296, 1692–1694 (2002).CAS 
    PubMed 
    Article 

    Google Scholar 
    Hinder, S. L. et al. Changes in marine dinoflagellate and diatom abundance under climate change. Nat. Clim. Change 2, 271–275 (2012).Article 

    Google Scholar 
    Southward, A. J., Hawkins, S. J. & Burrows, M. T. Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. J. Therm. Biol. 20, 127–155 (1995).Article 

    Google Scholar 
    Fenton, I. S. et al. Triton, a new species-level database of Cenozoic planktonic foraminiferal occurrences. Sci. Data 8, 160 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kucera, M., Rosell-Melé, A., Schneider, R., Waelbroeck, C. & Weinelt, M. Multiproxy approach for the reconstruction of the glacial ocean surface (MARGO). Quat. Sci. Rev. 24, 813–819 (2005).Kucera, M. et al. Reconstruction of sea-surface temperatures from assemblages of planktonic foraminifera: multi-technique approach based on geographically constrained calibration data sets and its application to glacial Atlantic and Pacific Oceans. Quat. Sci. Rev. 24, 951–998 (2005).Article 

    Google Scholar 
    Siccha, M. & Kucera, M. ForCenS, a curated database of planktonic foraminifera census counts in marine surface sediment samples. Sci. Data 4, 170109 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ezard, T. H. G., Aze, T., Pearson, P. N. & Purvis, A. Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science 332, 349–351 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    Fenton, I. S. et al. The impact of Cenozoic cooling on assemblage diversity in planktonic foraminifera. Phil. Trans. R. Soc. B 371, 20150224 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Lowery, C. M. & Fraass, A. J. Morphospace expansion paces taxonomic diversification after end Cretaceous mass extinction. Nat. Ecol. Evol. 3, 900–904 (2019).PubMed 
    Article 

    Google Scholar 
    Wade, B. S., Pearson, P. N., Berggren, W. A. & Pälike, H. Review and revision of Cenozoic tropical planktonic foraminiferal biostratigraphy and calibration to the geomagnetic polarity and astronomical time scale. Earth Sci. Rev. 104, 111–142 (2011).Article 

    Google Scholar 
    Antell, G. S., Fenton, I. S., Valdes, P. J. & Saupe, E. E. Thermal niches of planktonic foraminifera are static throughout glacial-interglacial climate change. Proc. Natl. Acad. Sci. USA https://doi.org/10.1073/pnas.2017105118 (2021).Fauth, J. E. et al. Simplifying the jargon of community ecology: a conceptual approach. Am. Nat. 147, 282–286 (1996).Article 

    Google Scholar 
    Jackson, S. T. & Overpeck, J. T. Responses of plant populations and communities to environmental changes of the late Quaternary. Paleobiology 26, 194–220 (2000).Article 

    Google Scholar 
    Bard, E., Rostek, F., Turon, J.-L. & Gendreau, S. Hydrological impact of Heinrich events in the subtropical Northeast Atlantic. Science 289, 1321–1324 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    Broecker, W. S. Massive iceberg discharges as triggers for global climate change. Nature 372, 421–424 (1994).CAS 
    Article 

    Google Scholar 
    Ruddiman, W. F. Late Quaternary deposition of ice-rafted sand in the subpolar North Atlantic (lat 40° to 65°N). Geol. Soc. Am. Bull. 88, 1813–1827 (1977).Article 

    Google Scholar 
    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, 2001).Liow, L. H., Van Valen, L. & Stenseth, N. C. Red Queen: from populations to taxa and communities. Trends Ecol. Evol. 26, 349–358 (2011).PubMed 
    Article 

    Google Scholar 
    Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).Article 

    Google Scholar 
    Jackson, S. T. & Sax, D. F. Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol. Evol. 25, 153–160 (2010).PubMed 
    Article 

    Google Scholar 
    Williams, J. W., Ordonez, A. & Svenning, J. C. A unifying framework for studying and managing climate-driven rates of ecological change. Nat. Ecol. Evol. 5, 17–26 (2021).PubMed 
    Article 

    Google Scholar 
    Van Meerbeeck, C. J., Renssen, H. & Roche, D. M. How did Marine Isotope Stage 3 and Last Glacial Maximum climates differ? Perspectives from equilibrium simulations. Clim. Past 5, 33–51 (2009).Article 

    Google Scholar 
    Jonkers, L. & Kučera, M. Global analysis of seasonality in the shell flux of extant planktonic Foraminifera. Biogeosciences 12, 2207–2226 (2015).Article 

    Google Scholar 
    Ofstad, S. et al. Development, productivity, and seasonality of living planktonic foraminiferal faunas and Limacina helicina in an area of intense methane seepage in the Barents Sea. J. Geophys. Res. Biogeosci. 125, e2019JG005387 (2020).CAS 
    Article 

    Google Scholar 
    Bova, S., Rosenthal, Y., Liu, Z., Godad, S. P. & Yan, M. Seasonal origin of the thermal maxima at the Holocene and the last interglacial. Nature 589, 548–553 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rillo, M. C. et al. On the mismatch in the strength of competition among fossil and modern species of planktonic Foraminifera. Glob. Ecol. Biogeogr. 28, 1866–1878 (2019).Article 

    Google Scholar 
    Lisiecki, L. E. & Stern, J. V. Regional and global benthic δ18O stacks for the last glacial cycle. Paleoceanography 31, 1368–1394 (2016).Article 

    Google Scholar 
    Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013).CAS 
    Article 

    Google Scholar 
    Butzin, M., Köhler, P. & Lohmann, G. Marine radiocarbon reservoir age simulations for the past 50,000 years. Geophys. Res. Lett. 44, 8473–8480 (2017).CAS 
    Article 

    Google Scholar 
    Langner, M. & Mulitza, S. Technical Note: PaleoDataView—A software toolbox for the collection, homogenization and visualization of marine proxy data. Clim 15, 2067–2072 (2019).
    Google Scholar 
    Mix, A. C., Bard, E. & Schneider, R. Environmental processes of the ice age: land, oceans, glaciers (EPILOG). Quat. Sci. Rev. 20, 627–657 (2001).Article 

    Google Scholar 
    Osman, M. B. et al. Globally resolved surface temperatures since the Last Glacial Maximum. Nature 599, 239–244 (2021).CAS 
    PubMed 
    Article 

    Google Scholar 
    Horn, H. S. Measurement of ‘overlap’ in comparative ecological studies. Am. Nat. 100, 419–424 (1966).Article 

    Google Scholar 
    Jost, L., Chao, A. & Chazdon, R. L. in Biological diversity: frontiers in measurement and assessment (eds Anne E. Magurran & Brian J. McGill) 66–84 (Oxford University Press, 2011).Ferrier, S., Manion, G., Elith, J. & Richardson, K. Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Divers. Distrib. 13, 252–264 (2007).Article 

    Google Scholar 
    Shannon, C. E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948).Article 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).Article 

    Google Scholar 
    Firke, S. janitor: Simple tools for examining and cleaning dirty data. R package version 2.1.0 https://CRAN.R-project.org/package=janitor (2021).Oksanen, J. et al. vegan: Community ecology package. R package version 2.5-7 https://CRAN.R-project.org/package=vegan (2020).Hallett, L. M. et al. codyn: an R package of community dynamics metrics. Methods Ecol. Evol. 7, 1146–1151 (2016).Article 

    Google Scholar 
    Juggins, S. rioja: Analysis of quaternary science data. R package version 0.9-26 https://cran.r-project.org/package=rioja (2020).Lê, S., Josse, J. & Husson, F. FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1–18 (2008).Article 

    Google Scholar 
    Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).Hijmans, R. J. raster: Geographic data analysis and modeling. R package version 3.4-13 https://CRAN.R-project.org/package=raster (2021).Garnier, S. viridis: Default color maps from ‘matplotlib’. R package version 0.6.1 https://CRAN.R-project.org/package=viridis (2021.)Locarnini, R. A. et al. World Ocean Atlas 2018, Vol. 1: Temperature. NOAA Atlas NESDIS 81 (NOAA, 2019). More