More stories

  • in

    Heterogeneous adaptive behavioral responses may increase epidemic burden

    Constant contacts modelWe assume the affected population is composed of two risk-groups, a fraction p of the population is composed of risk-takers (RT) and the remaining fraction (1-p) are risk-evaders (RE). We differentiate the RT and RE subpopulations by assuming the RE population face a reduced likelihood of infection due to adopting precautionary behaviors. On the other hand, we assume RT do not follow public health recommendations, thus facing a higher risk of infection, relative to the RE population. Political or ideological reasons, economic stress, the lack of reasonable alternatives, epidemic politicization or the lack of trust in public health authorities are some of the documented factors that potentially lead the population to risk the dangers of COVID-19 infection44, 45.Previous mathematical models consider complex within-host disease dynamics46 or the impact of exogenous factors on the COVID-19 transmission dynamics47. In this study, we focus on incorporating individual heterogeneous adaptive behavioral responses, based on group-specific infection risk perceptions. Our model of disease progression assumes that individuals in each behavioral group may show the following health status: Susceptible (S), infectious Exposed (E), Infectious symptomatic (I), infectious Asymptomatic (A), and Recovered (R). We consider a pre-symptomatic infectious health status (E), following evidence suggesting that exposed individuals exhibit a period of viral shedding38, 48,49,50,51. RT susceptible individuals ((S_1)) can get infected by making contacts with either: symptomatic ones (I) with a baseline per-contact likelihood of disease transmission (beta), exposed individuals ((E_1) and (E_2)) with reduced per-contact likelihood of infection (rho beta) , or asymptomatic individuals ((A_1) and (A_2)) with reduced per-contact likelihood of infection (alpha beta). Similarly RE susceptible individuals ((S_2)) may get infected by making contacts with symptomatic, exposed or asymptomatic individuals at respective likelihoods, (epsilon beta), (rho epsilon beta), and (alpha epsilon beta), where (0 More

  • in

    Sex differences in the winter activity of desert hedgehogs (Paraechinus aethiopicus) in a resource-rich habitat in Qatar

    Nagy, K. A. Field metabolic rate and food requirement scaling in mammals and birds. Ecol. Monogr. 57, 111–128 (1987).Article 

    Google Scholar 
    Anderson, K. J. & Jetz, W. The broad-scale ecology of energy expenditure of endotherms. Ecol. Lett. 8, 310–318 (2005).Article 

    Google Scholar 
    Terrien, J., Perret, M. & Aujard, F. Behavioral thermoregulation in mammals: A review. Front. Biosci. 16, 1428–1444 (2011).Article 

    Google Scholar 
    Mery, F. & Burns, J. G. Behavioural plasticity: An interaction between evolution and experience. Evol. Ecol. 24, 571–583 (2010).Article 

    Google Scholar 
    Brockmann, H. J. The evolution of alternative strategies and tactics. Adv. Study Behav. 30, 1–51 (2001).Article 

    Google Scholar 
    Milling, C. R., Rachlow, J. L., Johnson, T. R., Forbey, J. S. & Shipley, L. A. Seasonal variation in behavioral thermoregulation and predator avoidance in a small mammal. Behav. Ecol. 28, 1236–1247 (2017).Article 

    Google Scholar 
    Guiden, P. W. & Orrock, J. L. Seasonal shifts in activity timing reduce heat loss of small mammals during winter. Anim. Behav. 164, 181–192 (2020).Article 

    Google Scholar 
    Cotton, C. L. & Parker, K. L. Winter activity patterns of northern flying squirrels in sub-boreal forests. Can. J. Zool. 78, 1896–1901 (2000).Article 

    Google Scholar 
    Long, R. A., Martin, T. J. & Barnes, B. M. Body temperature and activity patterns in free-living arctic ground squirrels. J. Mammal. 86, 314–322 (2005).Article 

    Google Scholar 
    Zschille, J., Stier, N. & Roth, M. Gender differences in activity patterns of American mink Neovison vison in Germany. Eur. J. Wildl. Res. 56, 187–194 (2010).Article 

    Google Scholar 
    Geiser, F. Hibernation. Curr. Biol. 23, R188–R193 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    GĂŒr, M. K. & GĂŒr, H. Age and sex differences in hibernation patterns in free-living Anatolian ground squirrels. Mamm. Biol. 80, 265–272 (2015).Article 

    Google Scholar 
    Kisser, B. & Goodwin, H. T. Hibernation and overwinter body temperatures in free-ranging thirteen-lined ground squirrels, Ictidomys tridecemlineatus. Am. Midl. Nat. 167, 396–409 (2012).Article 

    Google Scholar 
    Dmi’el, R. & Schwarz, M. Hibernation patterns and energy expenditure in hedgehogs from semi-arid and temperate habitats. J. Comp. Physiol. B 155, 117–123 (1984).Article 

    Google Scholar 
    Abu Baker, M. A. et al. Caught basking in the winter sun: Preliminary data on winter thermoregulation in the Ethiopian hedgehog, Paraechinus aethiopicus in Qatar. J. Arid Environ. 125, 52–55 (2016).ADS 
    Article 

    Google Scholar 
    McKechnie, A. E. & Mzilikazi, N. Heterothermy in Afrotropical mammals and birds: A review. Integr. Comp. Biol. 51, 349–363 (2011).PubMed 
    Article 

    Google Scholar 
    Wacker, C. B., McAllan, B. M., Körtner, G. & Geiser, F. The role of basking in the development of endothermy and torpor in a marsupial. J. Comp. Physiol. B 187, 1029–1038 (2017).PubMed 
    Article 

    Google Scholar 
    Brown, K. J. & Downs, C. T. Basking behaviour in the rock hyrax (Procavia capensis) during winter. Afr. Zool. 42, 70–79 (2007).Article 

    Google Scholar 
    Humphries, M. M., Thomas, D. W. & Kramer, D. L. The role of energy availability in mammalian hibernation: A cost-benefit approach. Physiol. Biochem. Zool. 76, 165–179 (2003).PubMed 
    Article 

    Google Scholar 
    Field, K. A. et al. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol. Ecol. 27, 3727–3743 (2018).CAS 
    Article 

    Google Scholar 
    Bieber, C., Cornils, J. S., Hoelzl, F., Giroud, S. & Ruf, T. The costs of locomotor activity? Maximum body temperatures and the use of torpor during the active season in edible dormice. J. Comp. Physiol. B 187, 803–814 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Eto, T. et al. Individual variation of daily torpor and body mass change during winter in the large Japanese field mouse (Apodemus speciosus). J. Comp. Physiol. B 188, 1005–1014 (2018).PubMed 
    Article 

    Google Scholar 
    Zervanos, S. M., Maher, C. R. & Florant, G. L. Effect of body mass on hibernation strategies of woodchucks (Marmota monax). (2014).Ford, R. G. Home range in a patchy environment: Optimal foraging predictions. Am. Zool. 23, 315–326 (1983).Article 

    Google Scholar 
    Czenze, Z. J. & Willis, C. K. R. Warming up and shipping out: Arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). J. Comp. Physiol. B 185, 575–586 (2015).PubMed 
    Article 

    Google Scholar 
    Batavia, M., Nguyen, G., Harman, K. & Zucker, I. Hibernation patterns of Turkish hamsters: Influence of sex and ambient temperature. J. Comp. Physiol. B 183, 269–277 (2013).PubMed 
    Article 

    Google Scholar 
    Kato, G. A. et al. Individual differences in torpor expression in adult mice are related to relative birth mass. J. Exp. Biol. 221, jeb171983 (2018).PubMed 
    Article 

    Google Scholar 
    Williams, C. T. et al. Sex-dependent phenological plasticity in an arctic hibernator. Am. Nat. 190, 854–859 (2017).PubMed 
    Article 

    Google Scholar 
    Healy, J. E., Burdett, K. A., Buck, C. L. & Florant, G. L. Sex differences in torpor patterns during natural hibernation in golden-mantled ground squirrels (Callospermophilus lateralis). J. Mammal. 93, 751–758 (2012).Article 

    Google Scholar 
    Wang, Y., Yuan, L.-L., Peng, X., Wang, Y. & Yang, M. Experimental study on hibernation patterns in different ages and sexes of daurian ground squirrel (Spermophilus Dauricus). Shenyang Shifan Daxue Xuebao (Ziran Kexue Ban) 27, 351–355 (2009).
    Google Scholar 
    Siutz, C., Franceschini, C. & Millesi, E. Sex and age differences in hibernation patterns of common hamsters: Adult females hibernate for shorter periods than males. J. Comp. Physiol. B 186, 801–811 (2016).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Michener, G. R. Sexual differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernacula. Oecologia 89, 397–406 (1992).ADS 
    PubMed 
    Article 

    Google Scholar 
    Boyles, J. G., Bennett, N. C., Mohammed, O. B. & Alagaili, A. N. Torpor patterns in Desert Hedgehogs (Paraechinus aethiopicus) represent another new point along a thermoregulatory continuum. Physiol. Biochem. Zool. 90, 445–452 (2017).PubMed 
    Article 

    Google Scholar 
    Reeve, N. Hedgehogs (Poyser, 1994).
    Google Scholar 
    He, K. et al. An estimation of erinaceidae phylogeny: A combined analysis approach. PLoS One 7, e39304 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Schoenfeld, M. & Yom-Tov, Y. The biology of two species of hedgehogs, Erinaceus europaeus concolor and Hemiechinus auritus aegyptius, Israel. Mammalia 49, 339–356 (1985).Article 

    Google Scholar 
    Haigh, A., O’Riordan, R. M. & Butler, F. Nesting behaviour and seasonal body mass changes in a rural Irish population of the Western hedgehog (Erinaceus europaeus). Acta Theriol. (Warsz) 57, 321–331 (2012).Article 

    Google Scholar 
    Rasmussen, S. L., Berg, T. B., Dabelsteen, T. & Jones, O. R. The ecology of suburban juvenile European hedgehogs (Erinaceus europaeus) in Denmark. Ecol. Evol. 9, 13174–13187 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Jensen, A. B. Overwintering of European hedgehogs (Erinaceus europaeus) in a Danish rural area. Acta Theriol. (Warsz) 49, 145–155 (2004).Article 

    Google Scholar 
    Jackson, D. B. The breeding biology of introduced hedgehogs (Erinaceus europaeus) on a Scottish Island: Lessons for population control and bird conservation. J. Zool. 268, 303–314 (2006).Article 

    Google Scholar 
    Rautio, A., Valtonen, A., Auttila, M. & Kunnasranta, M. Nesting patterns of European hedgehogs (Erinaceus europaeus) under northern conditions. Acta Theriol. (Warsz) 59, 173–181 (2014).Article 

    Google Scholar 
    Hallam, S. L. & Mzilikazi, N. Heterothermy in the southern African hedgehog, Atelerix frontalis. J. Comp. Physiol. B 181, 437–445 (2011).PubMed 
    Article 

    Google Scholar 
    South, K. E., Haynes, K. & Jackson, A. C. Hibernation Patterns of the European Hedgehog, Erinaceus europaeus, at a Cornish Rescue Centre. Animals 10, 1418 (2020).PubMed Central 
    Article 

    Google Scholar 
    Gillies, A. C., Ellison, G. T. H. & Skinner, J. D. The effect of seasonal food restriction on activity, metabolism and torpor in the South African hedgehog (Atelerix frontalis). J. Zool. 223, 117–130 (1991).Article 

    Google Scholar 
    Gazzard, A. & Baker, P. J. Patterns of feeding by householders affect activity of hedgehogs (Erinaceus europaeus) during the hibernation period. Animals 10, 1344 (2020).PubMed Central 
    Article 

    Google Scholar 
    Dmiel, R. & Schwarz, M. Hibernation patterns and energy expenditure in hedgehogs from semi-arid and temperate habitats. J. Comp. Physiol. B 155, 117–123 (1984).Article 

    Google Scholar 
    Fowler, P. A. & Racey, P. A. Daily and seasonal cycles of body temperature and aspects of heterothermy in the hedgehog Erinaceus europaeus. J. Comp. Physiol. B 160, 299–307 (1990).CAS 
    PubMed 
    Article 

    Google Scholar 
    Rutovskaya, M. V. et al. The dynamics of body temperature of the Eastern European hedgehog (Erinaceus roumanicus) during winter hibernation. Biol. Bull. 46, 1136–1145 (2019).Article 

    Google Scholar 
    Harrison, D. L. & Bates, P. J. J. The Mammals of Arabia Vol 354 (Harrison Zoological Museum Sevenoaks, 1991).
    Google Scholar 
    Al-Musfir, H. M. & Yamaguchi, N. Timings of hibernation and breeding of Ethiopian Hedgehogs, Paraechinus aethiopicus in Qatar. Zool. Middle East 45, 3–10 (2008).Article 

    Google Scholar 
    Pettett, C. E., Al-Hajri, A., Al-Jabiry, H., Macdonald, D. W. & Yamaguchi, N. A comparison of the Ranging behaviour and habitat use of the Ethiopian hedgehog (Paraechinus aethiopicus) in Qatar with hedgehog taxa from temperate environments. Sci. Rep. 8, 1–10 (2018).Article 
    CAS 

    Google Scholar 
    Abu Baker, M. A., Reeve, N., Conkey, A. A. T., Macdonald, D. W. & Yamaguchi, N. Hedgehogs on the move: Testing the effects of land use change on home range size and movement patterns of free-ranging Ethiopian hedgehogs. PLoS One 12, e0180826 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Yamaguchi, N., Al-Hajri, A. & Al-Jabiri, H. Timing of breeding in free-ranging Ethiopian hedgehogs, Paraechinus aethiopicus, from Qatar. J. Arid Environ. 99, 1–4 (2013).ADS 
    Article 

    Google Scholar 
    Alagaili, A. N., Bennett, N. C., Mohammed, O. B. & Hart, D. W. The reproductive biology of the Ethiopian hedgehog, Paraechinus aethiopicus, from central Saudi Arabia: The role of rainfall and temperature. J. Arid Environ. 145, 1–9 (2017).ADS 
    Article 

    Google Scholar 
    Pettett, C. E. et al. Daily energy expenditure in the face of predation: Hedgehog energetics in rural landscapes. J. Exp. Biol. 220, 460–468 (2017).PubMed 
    Article 

    Google Scholar 
    Kraus, C., Eberle, M. & Kappeler, P. M. The costs of risky male behaviour: Sex differences in seasonal survival in a small sexually monomorphic primate. Proc. R. Soc. B Biol. Sci. 275, 1635–1644 (2008).Article 

    Google Scholar 
    Mzilikazi, N. & Lovegrove, B. G. Reproductive activity influences thermoregulation and torpor in pouched mice, Saccostomus campestris. J. Comp. Physiol. B 172, 7–16 (2002).PubMed 
    Article 

    Google Scholar 
    Richter, M. M., Barnes, B. M., O’reilly, K. M., Fenn, A. M. & Buck, C. L. The influence of androgens on hibernation phenology of free-living male arctic ground squirrels. Horm. Behav. 89, 92–97 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    Haigh, A., Butler, F. & O’Riordan, R. M. Courtship behaviour of western hedgehogs (Erinaceus europaeus) in a rural landscape in Ireland and the first appearance of offspring. Lutra 55, 41–54 (2012).
    Google Scholar 
    Nicol, S. C., Morrow, G. E. & Harris, R. L. Energetics meets sexual conflict: The phenology of hibernation in Tasmanian echidnas. Funct. Ecol. 33, 2150–2160 (2019).Article 

    Google Scholar 
    Pettett, C. W., Macdonald, D., Al-Hajiri, A., Al-Jabiry, H. & Yamaguchi, N. Characteristics and demography of a free-ranging Ethiopian Hedgehog, Paraechinus aethiopicus, population in Qatar. Animals 10, 951 (2020).PubMed Central 
    Article 

    Google Scholar 
    Kenward, R. E. A Manual for Wildlife Radio Tagging (Academic Press, 2000).
    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Core Team, 2021).
    Google Scholar 
    Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage, 2019).
    Google Scholar  More

  • in

    Individual variability in foraging success of a marine predator informs predator management

    Krause, M. & Robins, K. Charismatic species and beyond: How cultural schemas and organisational routines shape conservation. Conserv. Soc. 15, 313–321 (2017).
    Google Scholar 
    Marshall, K. N., Stier, A. C., Samhouri, J. F., Kelly, R. P. & Ward, E. J. Conservation challenges of predator recovery. Conserv. Lett. 9, 70–78 (2016).
    Google Scholar 
    Bearzi, G., Holcer, D. & Di Sciara, G. N. The role of historical dolphin takes and habitat degradation in shaping the present status of northern Adriatic cetaceans. Aquat. Conserv. Mar. Freshw. Ecosyst. 14, 363–379 (2004).
    Google Scholar 
    Lavigne, D. M. Marine mammals and fisheries: The role of science in the culling debate. In Marine Mammals: Fisheries Tourism and Management Issues (eds Gales, N. et al.) 31–47 (CSIRO Publishing, 2003).
    Google Scholar 
    Bowen, W. D. & Lidgard, D. Marine mammal culling programs: Review of effects on predator and prey populations. Mamm. Rev. 43, 207–220 (2013).
    Google Scholar 
    SvanbĂ€ck, R. & Persson, L. Individual diet specialization, niche width and population dynamics: Implications for trophic polymorphisms. J. Anim. Ecol. 73, 973–982 (2004).
    Google Scholar 
    Butler, J. R. A. et al. The Moray Firth Seal Management Plan: An adaptive framework for balancing the conservation of seals, salmon, fisheries and wildlife tourism in the UK. Aquat. Conserv. Mar. Freshw. Ecosyst. 18, 1025–1038 (2008).
    Google Scholar 
    Graham, I. M., Harris, R. N., Matejusová, I. & Middlemas, S. J. Do ‘rogue’ seals exist? Implications for seal conservation in the UK. Anim. Conserv. 14, 587–598 (2011).
    Google Scholar 
    Linnell, J. D. C., Aanes, R., Swenson, J. E., Odden, J. & Smith, M. E. Large carnivores that kill livestock: Do ‘problem individuals’ really exist?. Wildl. Soc. Bull. 27, 698–705 (1999).
    Google Scholar 
    Tidwell, K. S., van der Leeuw, B. K., Magill, L. N., Carrothers, B. A. & Wertheimer, R. H. Evaluation of pinniped predation on adult salmonids and other fish in the Bonneville Dam tailrace (2017).Guillemette, M. & Brousseau, P. Does culling predatory gulls enhance the productivity of breeding common terns?. J. Appl. Ecol. 38, 1–8 (2001).
    Google Scholar 
    Rudolf, V. H. W. & Rasmussen, N. L. Population structure determines functional differences among species and ecosystem processes. Nat. Commun. 4, 2318 (2013).ADS 
    PubMed 

    Google Scholar 
    Harmon, L. J. et al. Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458, 1167–1170 (2009).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Adams, J. et al. A century of Chinook salmon consumption by marine mammal predators in the Northeast Pacific Ocean. Ecol. Inform. 34, 44–51 (2016).
    Google Scholar 
    Chasco, B. et al. Competing tradeoffs between increasing marine mammal predation and fisheries harvest of Chinook salmon. Sci. Rep. 7, 1–14 (2017).CAS 

    Google Scholar 
    Bearhop, S. et al. Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar. Ecol. Prog. Ser. 311, 157–164 (2006).ADS 

    Google Scholar 
    Thiemann, G. W., Iverson, S. J., Stirling, I. & Obbard, M. E. Individual patterns of prey selection and dietary specialization in an Arctic marine carnivore. Oikos 120, 1469–1478 (2011).
    Google Scholar 
    Königson, S., FjĂ€lling, A., Berglind, M. & Lunneryd, S. G. Male gray seals specialize in raiding salmon traps. Fish. Res. 148, 117–123 (2013).
    Google Scholar 
    Sih, A., Sinn, D. L. & Patricelli, G. L. On the importance of individual differences in behavioural skill. Anim. Behav. 155, 307–317 (2019).
    Google Scholar 
    Bjorkland, R. H. et al. Stable isotope mixing models elucidate sex and size effects on the diet of a generalist marine predator. Mar. Ecol. Prog. Ser. 526, 213–225 (2015).ADS 

    Google Scholar 
    Schwarz, D. et al. Large-scale molecular diet analysis in a generalist marine mammal reveals male preference for prey of conservation concern. Ecol. Evol. 8, 9889–9905 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Tinker, M. T., Costa, D. P., Estes, J. A. & Wieringa, N. Individual dietary specialization and dive behaviour in the California sea otter: Using archival time-depth data to detect alternative foraging strategies. Deep. Res. Part II Top. Stud. Oceanogr. 54, 330–342 (2007).ADS 

    Google Scholar 
    Voelker, M. R., Schwarz, D., Thomas, A., Nelson, B. W. & Acevedo-GutiĂ©rrez, A. Large-scale molecular barcoding of prey DNA reveals predictors of intrapopulation feeding diversity in a marine predator. Ecol. Evol. 10, 9867–9885 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Bolnick, D. I. et al. The ecology of individuals: Incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).MathSciNet 
    PubMed 

    Google Scholar 
    Harcourt, R. Individual variation in predation on fur seals by southern sea lions (Otaria byronia) in Peru. Can. J. Zool. 71, 1908–1911 (1993).
    Google Scholar 
    Marine Mammal Commission. Marine Mammal Protection Act. Marine Mammal Protection Act Amendment 1–56 (U.S. Fish and Wildlife Service, 2004). https://doi.org/10.1002/tcr.201190008.Book 

    Google Scholar 
    National Marine Fisheries Service. Willamette Falls Pinniped-Fishery Interaction Task Force Marine Mammal Protection Act, Section 120 (National Marine Fisheries Service, 2018).
    Google Scholar 
    Jefferson, T. A., Smultea, M. A., Ward, E. J. & Berejikian, B. Estimating the stock size of harbor seals (Phoca vitulina richardii) in the inland waters of Washington State using line-transect methods. PLoS ONE 16, e0241254 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jeffries, S., Huber, H., Calambokidis, J. & Laake, J. Trends and status of harbor seals in Washington State: 1978–1999. J. Wildl. Manag. 67, 208–219 (2003).
    Google Scholar 
    Thomas, A. C., Lance, M. M., Jeffries, S. J., Miner, B. G. & Acevedo-GutiĂ©rrez, A. Harbor seal foraging response to a seasonal resource pulse, spawning Pacific herring. Mar. Ecol. Prog. Ser. 441, 225–239 (2011).ADS 

    Google Scholar 
    Chasco, B. et al. Estimates of chinook salmon consumption in Washington State inland waters by four marine mammal predators from 1970 to 2015. Can. J. Fish. Aquat. Sci. 74, 1173–1194 (2017).
    Google Scholar 
    Farrer, J. & Acevedo-GutiĂ©rrez, A. Use of haul-out sites by harbor seals (Phoca vitulina) in Bellingham: Implications for future development. Northwest. Nat. 91, 74–79 (2010).
    Google Scholar 
    Steingass, S., Jeffries, S., Hatch, D. & Dupont, J. Field report: 2020 pinniped research and management activities at Bonneville Dam (2020).Tidwell, K. S., Carrothers, B. A., Blumstein, D. T. & Schakner, Z. A. Steller sea lion (Eumetopias jubatus) response to non-lethal hazing at Bonneville Dam. Front. Conserv. Sci. 2, 1–9 (2021).
    Google Scholar 
    Hiruki, L. M., Schwartz, M. K. & Boveng, P. L. Hunting and social behaviour of leopard seals (Hydrurga leptonyx) at Seal Island, South Shetland Islands, Antarctica. J. Zool. 249, 97–109 (1999).
    Google Scholar 
    Ainley, D. G., Ballard, G., Karl, B. J. & Dugger, K. M. Leopard seal predation rates at penguin colonies of different size. Antarct. Sci. 17, 335–340 (2005).ADS 

    Google Scholar 
    Páez-Rosas, D. et al. Hunting and cooperative foraging behavior of Galapagos sea lion: An attack to large pelagics. Mar. Mammal Sci. 36, 386–391 (2020).
    Google Scholar 
    Macneale, K. H., Kiffney, P. M. & Scholz, N. L. Pesticides, aquatic food webs, and the conservation of Pacific salmon. Front. Ecol. Environ. 8, 475–482 (2010).
    Google Scholar 
    Roni, P., Anders, P. J., Beechie, T. J. & Kaplowe, D. J. Review of tools for identifying, planning, and implementing habitat restoration for Pacific salmon and steelhead. North Am. J. Fish. Manag. 38, 355–376 (2018).
    Google Scholar 
    Morissette, L., Christensen, V. & Pauly, D. Marine mammal impacts in exploited ecosystems: Would large scale culling benefit fisheries?. PLoS ONE 7, 1–18 (2012).
    Google Scholar 
    Thompson, D., Coram, A. J., Harris, R. N. & Sparling, C. E. Review of non-lethal seal control options to limit seal predation on salmonids in rivers and at finfish farms. Scott. Mar. Freshw. Sci. 12, 137 (2021).
    Google Scholar 
    Dickinson, J. L., Zuckerberg, B. & Bonter, D. N. Citizen science as an ecological research tool: Challenges and benefits. Annu. Rev. Ecol. Evol. Syst. 41, 149–172 (2010).
    Google Scholar 
    Fairbanks, C. & Penttila, D. Bellingham Bay Forage Fish Spawning Assessment (2016).Madsen, S. W. & Nightengale, T. Whatcom Creek Ten-Years After: Summary Report (Department of Public Works, 2009). https://doi.org/10.2307/j.ctt20krzd7.7.Book 

    Google Scholar 
    Martin, P. & Bateson, P. Measuring Behaviour: An Introductory Guide (Cambridge University Press, 2007).
    Google Scholar 
    Bolger, D. T., Morrison, T. A., Vance, B., Lee, D. & Farid, H. A computer-assisted system for photographic mark-recapture analysis. Methods Ecol. Evol. 3, 813–822 (2012).
    Google Scholar 
    Harrison, P. J. et al. Incorporating movement into models of grey seal population dynamics. J. Anim. Ecol. 75, 634–645 (2006).PubMed 

    Google Scholar 
    Thompson, P. M. & Wheeler, H. Photo-ID-based estimates of reproductive patterns in female harbor seals. Mar. Mammal Sci. 24, 138–146 (2008).
    Google Scholar 
    Washington Department of Fish and Wildlife. Whatcom Creek Hatchery (WDFW, 2019).
    Google Scholar 
    R Core Team. R: A language and environment for statistical computing (R Core Team, 2020).
    Google Scholar 
    Bates, D., MÀchler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).Article 

    Google Scholar 
    Lloyd-Smith, J. O. Maximum likelihood estimation of the negative binomial dispersion parameter for highly overdispersed data, with applications to infectious diseases. PLoS ONE 2, 1–8 (2007).
    Google Scholar 
    Zhang, D. rsq: R-Squared and Related Measures. R package version 2.1 (2020).LĂŒdecke, D., Ben-Shachar, M., Patil, I., Waggoner, P. & Makowski, D. Performance: An R package for assessment, comparison and testing of statistical models. J. Open Source Softw. 6, 3139 (2021).ADS 

    Google Scholar 
    Bolker, B. M. et al. Generalized linear mixed models: A practical guide for ecology and evolution. Trends Ecol. Evol. 24, 127–135 (2009).PubMed 

    Google Scholar 
    Zuur, A. F., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, 2009). https://doi.org/10.1007/978-0-387-87458-6.Book 
    MATH 

    Google Scholar  More

  • in

    Hydrologic regime alteration and influence factors in the Jialing River of the Yangtze River, China

    Ge, J., Peng, W., Wei, H. W., Qu, X. & Singh, S. Quantitative assessment of flow regime alteration using a revised range of variability methods. Water 10(5), 597 (2018).Article 

    Google Scholar 
    Latrubesse, E. M. et al. Damming the rivers of the Amazon basin. Nature 546(7658), 363–369 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    Meade, R. H. & Moody, J. A. Causes for the decline of suspended-sediment discharge in the Mississippi River system, 1940–2007. Hydrol. Process 24(1), 35–49 (2010).
    Google Scholar 
    Fathi, M. M., Awadallah, A. G., Abdelbaki, A. M. & Haggag, M. A new Budyko framework extension using time series SARIMAX model. J. Hydrol. 570(2019), 827–838 (2019).ADS 
    Article 

    Google Scholar 
    Wang, H., Liu, J. & Guo, W. The variation and attribution analysis of the runoff and sediment in the lower reach of the Yellow River during the past 60 years. Water Supply 21(6), 3193–3209 (2021).Article 

    Google Scholar 
    Guo, S. L., Guo, J., Hou, Y., Xiong, L. & Hong, X. Prediction of future runoff change based on Budyko hypothesis in Yangtze River basin. Adv. Water Sci. 26(02), 151–160 (2015).
    Google Scholar 
    Zhang, X., Dong, Z., Gupta, H., Wu, G. & Li, D. Impact of the three gorges dam on the hydrology and ecology of the Yangtze River. Water 590(8), 1–18 (2016).ADS 
    CAS 

    Google Scholar 
    Zhang, J., Zhang, M., Song, Y. & Lai, Y. Hydrological simulation of the Jialing River Basin using the MIKE SHE model in changing climate. J. Water Clim. Change 12(6), 1–20 (2021).
    Google Scholar 
    Richter, B. D., Baumgartner, J. V., Powell, J. & Braun, P. D. A method for assessing hydrologic alteration within ecosystems. Conserv. Biol. 10(4), 1163–1174 (1996).Article 

    Google Scholar 
    Richter, B. D., Baumgartner, J. V., Wigington, B. & Braun, D. How much water does a river need?. Freshw. Biol. 37(1), 231–249 (1997).Article 

    Google Scholar 
    Richter, B. D., Baumgartner, J. V., Braun, D. P. & Powell, J. A spatial assessment of hydrologic alteration within a river network. Regul. River Res. Manag. 14(4), 329–340 (1998).Article 

    Google Scholar 
    Guo, W., Xu, G., Shao, J., Bing, J. & Chen, X. Research on the middle and lower reaches of the Yangtze River and lake’s hydrological alterations based on RVA. In IOP Conference Series: Earth and Environmental Science Vol 153, No 6, 062047.1–062047.8 (2018).Guo, W., Li, Y., Wang, H. & Zha, H. Assessment of eco-hydrological regime of lower reaches of Three Gorges Reservoir based on IHA-RVA. Resour. Environ. Yangtze Basin 27(09), 2014–2021 (2018).
    Google Scholar 
    Zuo, Q. & Liang, S. Effects of dams on river flow regime based on IHA/RVA. Proc. Int. Assoc. Hydrol. Sci. 368(368), 275–276 (2015).
    Google Scholar 
    Mwedzi, T., Katiyo, L., Mugabe, F. T., Bere, T. & Kuoika, O. L. A spatial assessment of stream-flow characteristics and hydrologic alterations, post dam construction in the Manyame catchment, Zimbabwe. Water Sa 42(2), 194–202 (2016).CAS 
    Article 

    Google Scholar 
    Liu, J., Chen, J., Xu, J., Lin, Y. & Zhou, M. Attribution of runoff variation in the headwaters of the Yangtze River based on the Budyko hypothesis. Int. J. Environ. Res. Public Health 16(14), 2506.1-2506.15 (2019).
    Google Scholar 
    Yan, D. Using budyko-type equations for separating the impacts of climate and vegetation change on runoff in the source area of the yellow river. Water 12(12), 3418.1-3418.15 (2020).ADS 

    Google Scholar 
    Gunkel, A. & Lange, J. Water scarcity, data scarcity and the Budyko curve—An application in the Lower Jordan River Basin. J. Hydrol. Reg. Stud. 12(C), 136–149 (2017).Article 

    Google Scholar 
    Fathi, M. M., Awadallah, A. G., Abdelbaki, A. M. & Haggag, M. A new Budyko framework extension using time series SARIMAX model. J. Hydrol. 570, 827–838 (2019).ADS 
    Article 

    Google Scholar 
    Li, Y., Fan, J. & Liao, Y. Variation characteristics of streamflow and sediment in the Jialing river basin in the past 60 years. Mt. Res. 38(03), 339–348 (2020).
    Google Scholar 
    Liu, Y., Li, F. & Xu, X. Impacts of hydropower development on hydrological regime in mainstream of mid-lower Jialing River. Yangtze River 45(05), 10–15 (2014).
    Google Scholar 
    Zhou, Y. et al. Distinguishing the multiple controls on the decreased sediment flux in the Jialing River basin of the Yangtze River, Southwestern China. CATENA 193(C), 104593.1-104593.11 (2020).
    Google Scholar 
    Zeng, X. et al. Changes and relationships of climatic and hydrological droughts in the Jialing River Basin, China. PLoS ONE 10(11), e0141648 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Yan, M., Fang, G. H., Dai, L. H., Tan, Q. F. & Huang, X. F. Optimizing reservoir operation considering downstream ecological demands of water quantity and fluctuation based on IHA parameters. J. Hydrol. 4(2021), 126647 (2021).Article 

    Google Scholar 
    Wei, R., Liu, J., Zhang, T., Zeng, Q. & Dong, X. Attribution analysis of runoff variation in the upper-middle reaches of Yalong river. Resour. Environ. Yangtze Basin 29(07), 1643–1652 (2020).
    Google Scholar 
    Xie, J. H., Yu, J. H., Chem, H. S. & Hsu, P. C. Sources of subseasonal prediction skill for heatwaves over the Yangtze river basin revealed from three S2S models. Adv. Atmos. Sci. 37(12), 1435–1450 (2020).Article 

    Google Scholar 
    Guo, W., Li, Y., Wang, H. & Cha, H. Temporal variations and influencing factors of river runoff and sediment regimes in the Yangtze River, China. Desalin. Water Treat. 174(2020), 258–270 (2020).Article 

    Google Scholar 
    Tian, X. et al. Hydrologic alteration and possible underlying causes in the Wuding River, China. Sci. Total Environ. 693, 133556.1-133556.9 (2019).Article 
    CAS 

    Google Scholar 
    Tang, B., Wang, W. C. & Fan, X. Study on the influence of reservoir dispatch of the upper Yangtze river on the runoff control. E3S Web Conf. 283(18), 01030 (2021).
    Google Scholar 
    Liu, Y. et al. Characteristics and resource status of main commercial fish in the middle reaches of Jialing River, China. J. Appl. Environ. Biol. 27(04), 837–847 (2021).
    Google Scholar 
    Sun, Z., Zhang, M. & Chen, Y. Protection of the rare and endemic fish in the conservation area located in the upstream of the Yangtze River. Freshw. Fish. 44(06), 3–8 (2014).
    Google Scholar 
    Chen, Q. H. et al. Impacts of climate change and LULC change on runoff in the Jinsha River Basin. J. Geogr. Sci. 30(01), 85–102 (2020).Article 

    Google Scholar 
    Cui, L., Wang, Z. & Deng, L. Vegetation dynamics based on NDVI in Yangtze River Basin (China) during 1982–2015. IOP Conf. Ser. Materials Sci. Eng. 780(2020), 062049 (2020).Article 

    Google Scholar 
    Wang, Y., Wang, S., Wu, M. & Wang, S. Impacts of the land use and climate changes on the hydrological characteristics of Jialing River Basin. Res. Soil Water Conserv. 26(01), 135–142 (2019).
    Google Scholar 
    Wu, Y. L. & Pu, H. W. Y. The influence of hydropower station on sand content detection in Jialing River. Technol. Dev. Enterp. 38(9), 55–58 (2019).
    Google Scholar 
    Zhuo, Z., Qian, Z., Jiang, H., Wang, H. & Guo, W. Evaluation of hydrological regime in Xiangjiang basin on IHA-RVA method. China Rural Water Hydropower 8(2020), 188–192 (2020).
    Google Scholar 
    Chen, L. et al. Temporal characteristics detection and attribution analysis of hydrological time-series variation in the seagoing river of southern China under environmental change. Acta Geophys. 66(5), 1151–1170 (2018).ADS 
    Article 

    Google Scholar 
    Zhang, R., Liu, J., Mao, G. & Wang, L. Flow regime alterations of upper Heihe River based on improved RVA. Arid Zone Res. 38(01), 29–38 (2021).
    Google Scholar 
    Sun, Y. & Wang, X. Changes in runoff and driving force analysis in the key section of the Yellow River diversion project. J. Hydroecol. 41(06), 19–26 (2020).
    Google Scholar 
    Zhang, L., Dawes, W. R. & Walker, G. R. Response of mean annual evapotranspiration to vegetation changes at catchment scale. Water Resour. Res. 37(3), 701–708 (2001).ADS 
    Article 

    Google Scholar 
    Fu, B. Calculation of soil evaporation. Acta Meteor. Sin. 02(1981), 226–236 (1981).
    Google Scholar 
    Liu, J., Zhang, Q., Singh, V. P. & Shi, P. Contribution of multiple climatic variables and human activities to streamflow changes across China. J. Hydrol. 545(2016), 145–162 (2016).
    Google Scholar 
    Yang, D., Zhang, S. & Xu, X. Attribution analysis for runoff decline in Yellow River Basin during past fifty years based on Budyko hypothesis. Sci. Sinica 45(10), 1024–1034 (2015).
    Google Scholar 
    Schreiber, P. Ber die Beziehungen zwischen dem Niederschlag und der WasserfĂŒhrung der FlĂŒsse in Mitteleuropa. Meteorol. Z. 21, 441–452 (1904).Budyko, M. Evaporation under Natural Conditions (Gidrometeorizdat, Leningrad, Russia, 1948).Pike, J. The estimation of annual run-off from meteorological data in a tropical climate. J. Hydrol. 2, 116–123 (1964).Ol’dekop, E. On evaporation from the surface of river basins. Trans. Meteorol. Obs. 4, 200 (1911). More

  • in

    Found: hideout of some of the last primordial pigeons

    RESEARCH HIGHLIGHT
    01 July 2022

    Rock doves on some Scottish islands show almost no sign of having interbred with domestic pigeons.

    The relatively long, slender bill of this rock dove from the Outer Hebridean islands of Scotland are characteristic of feral pigeons’ ancestors. Credit: W. J. Smith et al./iScience

    .readcube-buybox { display: none !important;}
    Charles Darwin developed his theory of natural selection in part by studying a form of artificial selection: the nineteenth-century rage for pigeon breeding, which created a wealth of fantastical varieties of pigeon (Columba livia). So widespread was pigeon fancying that it seeded the world with escaped domestic birds and their feral descendants, which then hybridized with their wild ancestors, the rock doves.

    Access options

    /* style specs start */
    style{display:none!important}.LiveAreaSection-193358632 *{align-content:stretch;align-items:stretch;align-self:auto;animation-delay:0s;animation-direction:normal;animation-duration:0s;animation-fill-mode:none;animation-iteration-count:1;animation-name:none;animation-play-state:running;animation-timing-function:ease;azimuth:center;backface-visibility:visible;background-attachment:scroll;background-blend-mode:normal;background-clip:borderBox;background-color:transparent;background-image:none;background-origin:paddingBox;background-position:0 0;background-repeat:repeat;background-size:auto auto;block-size:auto;border-block-end-color:currentcolor;border-block-end-style:none;border-block-end-width:medium;border-block-start-color:currentcolor;border-block-start-style:none;border-block-start-width:medium;border-bottom-color:currentcolor;border-bottom-left-radius:0;border-bottom-right-radius:0;border-bottom-style:none;border-bottom-width:medium;border-collapse:separate;border-image-outset:0s;border-image-repeat:stretch;border-image-slice:100%;border-image-source:none;border-image-width:1;border-inline-end-color:currentcolor;border-inline-end-style:none;border-inline-end-width:medium;border-inline-start-color:currentcolor;border-inline-start-style:none;border-inline-start-width:medium;border-left-color:currentcolor;border-left-style:none;border-left-width:medium;border-right-color:currentcolor;border-right-style:none;border-right-width:medium;border-spacing:0;border-top-color:currentcolor;border-top-left-radius:0;border-top-right-radius:0;border-top-style:none;border-top-width:medium;bottom:auto;box-decoration-break:slice;box-shadow:none;box-sizing:border-box;break-after:auto;break-before:auto;break-inside:auto;caption-side:top;caret-color:auto;clear:none;clip:auto;clip-path:none;color:initial;column-count:auto;column-fill:balance;column-gap:normal;column-rule-color:currentcolor;column-rule-style:none;column-rule-width:medium;column-span:none;column-width:auto;content:normal;counter-increment:none;counter-reset:none;cursor:auto;display:inline;empty-cells:show;filter:none;flex-basis:auto;flex-direction:row;flex-grow:0;flex-shrink:1;flex-wrap:nowrap;float:none;font-family:initial;font-feature-settings:normal;font-kerning:auto;font-language-override:normal;font-size:medium;font-size-adjust:none;font-stretch:normal;font-style:normal;font-synthesis:weight style;font-variant:normal;font-variant-alternates:normal;font-variant-caps:normal;font-variant-east-asian:normal;font-variant-ligatures:normal;font-variant-numeric:normal;font-variant-position:normal;font-weight:400;grid-auto-columns:auto;grid-auto-flow:row;grid-auto-rows:auto;grid-column-end:auto;grid-column-gap:0;grid-column-start:auto;grid-row-end:auto;grid-row-gap:0;grid-row-start:auto;grid-template-areas:none;grid-template-columns:none;grid-template-rows:none;height:auto;hyphens:manual;image-orientation:0deg;image-rendering:auto;image-resolution:1dppx;ime-mode:auto;inline-size:auto;isolation:auto;justify-content:flexStart;left:auto;letter-spacing:normal;line-break:auto;line-height:normal;list-style-image:none;list-style-position:outside;list-style-type:disc;margin-block-end:0;margin-block-start:0;margin-bottom:0;margin-inline-end:0;margin-inline-start:0;margin-left:0;margin-right:0;margin-top:0;mask-clip:borderBox;mask-composite:add;mask-image:none;mask-mode:matchSource;mask-origin:borderBox;mask-position:0 0;mask-repeat:repeat;mask-size:auto;mask-type:luminance;max-height:none;max-width:none;min-block-size:0;min-height:0;min-inline-size:0;min-width:0;mix-blend-mode:normal;object-fit:fill;object-position:50% 50%;offset-block-end:auto;offset-block-start:auto;offset-inline-end:auto;offset-inline-start:auto;opacity:1;order:0;orphans:2;outline-color:initial;outline-offset:0;outline-style:none;outline-width:medium;overflow:visible;overflow-wrap:normal;overflow-x:visible;overflow-y:visible;padding-block-end:0;padding-block-start:0;padding-bottom:0;padding-inline-end:0;padding-inline-start:0;padding-left:0;padding-right:0;padding-top:0;page-break-after:auto;page-break-before:auto;page-break-inside:auto;perspective:none;perspective-origin:50% 50%;pointer-events:auto;position:static;quotes:initial;resize:none;right:auto;ruby-align:spaceAround;ruby-merge:separate;ruby-position:over;scroll-behavior:auto;scroll-snap-coordinate:none;scroll-snap-destination:0 0;scroll-snap-points-x:none;scroll-snap-points-y:none;scroll-snap-type:none;shape-image-threshold:0;shape-margin:0;shape-outside:none;tab-size:8;table-layout:auto;text-align:initial;text-align-last:auto;text-combine-upright:none;text-decoration-color:currentcolor;text-decoration-line:none;text-decoration-style:solid;text-emphasis-color:currentcolor;text-emphasis-position:over right;text-emphasis-style:none;text-indent:0;text-justify:auto;text-orientation:mixed;text-overflow:clip;text-rendering:auto;text-shadow:none;text-transform:none;text-underline-position:auto;top:auto;touch-action:auto;transform:none;transform-box:borderBox;transform-origin:50% 50%0;transform-style:flat;transition-delay:0s;transition-duration:0s;transition-property:all;transition-timing-function:ease;vertical-align:baseline;visibility:visible;white-space:normal;widows:2;width:auto;will-change:auto;word-break:normal;word-spacing:normal;word-wrap:normal;writing-mode:horizontalTb;z-index:auto;-webkit-appearance:none;-moz-appearance:none;-ms-appearance:none;appearance:none;margin:0}.LiveAreaSection-193358632{width:100%}.LiveAreaSection-193358632 .login-option-buybox{display:block;width:100%;font-size:17px;line-height:30px;color:#222;padding-top:30px;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-access-options{display:block;font-weight:700;font-size:17px;line-height:30px;color:#222;font-family:Harding,Palatino,serif}.LiveAreaSection-193358632 .additional-login >li:not(:first-child)::before{transform:translateY(-50%);content:””;height:1rem;position:absolute;top:50%;left:0;border-left:2px solid #999}.LiveAreaSection-193358632 .additional-login >li:not(:first-child){padding-left:10px}.LiveAreaSection-193358632 .additional-login >li{display:inline-block;position:relative;vertical-align:middle;padding-right:10px}.BuyBoxSection-683559780{display:flex;flex-wrap:wrap;flex:1;flex-direction:row-reverse;margin:-30px -15px 0}.BuyBoxSection-683559780 .box-inner{width:100%;height:100%}.BuyBoxSection-683559780 .readcube-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:1;flex-basis:255px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:300px;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .subscribe-buybox-nature-plus{background-color:#f3f3f3;flex-shrink:1;flex-grow:4;flex-basis:100%;background-clip:content-box;padding:0 15px;margin-top:30px}.BuyBoxSection-683559780 .title-readcube{display:block;margin:0;margin-right:20%;margin-left:20%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-buybox{display:block;margin:0;margin-right:29%;margin-left:29%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .title-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:24px;line-height:32px;color:#222;padding-top:30px;text-align:center;font-family:Harding,Palatino,serif}.BuyBoxSection-683559780 .asia-link{color:#069;cursor:pointer;text-decoration:none;font-size:1.05em;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:1.05em6}.BuyBoxSection-683559780 .access-readcube{display:block;margin:0;margin-right:10%;margin-left:10%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-asia-buybox{display:block;margin:0;margin-right:5%;margin-left:5%;font-size:14px;color:#222;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .access-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;padding-top:10px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .usps-buybox{display:block;margin:0;margin-right:30%;margin-left:30%;font-size:14px;color:#222;opacity:.8px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .price-buybox{display:block;font-size:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;padding-top:30px;text-align:center}.BuyBoxSection-683559780 .price-from{font-size:14px;padding-right:10px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:20px}.BuyBoxSection-683559780 .issue-buybox{display:block;font-size:13px;text-align:center;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:19px}.BuyBoxSection-683559780 .no-price-buybox{display:block;font-size:13px;line-height:18px;text-align:center;padding-right:10%;padding-left:10%;padding-bottom:20px;padding-top:30px;color:#222;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif}.BuyBoxSection-683559780 .vat-buybox{display:block;margin-top:5px;margin-right:20%;margin-left:20%;font-size:11px;color:#222;padding-top:10px;padding-bottom:15px;text-align:center;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;line-height:17px}.BuyBoxSection-683559780 .button-container{display:flex;padding-right:20px;padding-left:20px;justify-content:center}.BuyBoxSection-683559780 .button-container >*{flex:1px}.BuyBoxSection-683559780 .button-container >a:hover,.Button-505204839:hover,.Button-1078489254:hover,.Button-2808614501:hover{text-decoration:none}.BuyBoxSection-683559780 .readcube-button{background:#fff;margin-top:30px}.BuyBoxSection-683559780 .button-asia{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;margin-top:75px}.BuyBoxSection-683559780 .button-label-asia,.ButtonLabel-3869432492,.ButtonLabel-3296148077,.ButtonLabel-1566022830{display:block;color:#fff;font-size:17px;line-height:20px;font-family:-apple-system,BlinkMacSystemFont,”Segoe UI”,Roboto,Oxygen-Sans,Ubuntu,Cantarell,”Helvetica Neue”,sans-serif;text-align:center;text-decoration:none;cursor:pointer}.Button-505204839,.Button-1078489254,.Button-2808614501{background:#069;border:1px solid #069;border-radius:0;cursor:pointer;display:block;padding:9px;outline:0;text-align:center;text-decoration:none;min-width:80px;max-width:320px;margin-top:10px}.Button-505204839 .readcube-label,.Button-1078489254 .readcube-label,.Button-2808614501 .readcube-label{color:#069}
    /* style specs end */Subscribe to Nature+Get immediate online access to the entire Nature family of 50+ journals$29.99monthlySubscribe to JournalGet full journal access for 1 year$199.00only $3.90 per issueAll prices are NET prices.VAT will be added later in the checkout.Tax calculation will be finalised during checkout.Buy articleGet time limited or full article access on ReadCube.$32.00All prices are NET prices.

    Additional access options:

    doi: https://doi.org/10.1038/d41586-022-01780-2

    References

    Subjects

    Conservation biology

    Subjects

    Conservation biology More

  • in

    Houseflies harbor less diverse microbiota under laboratory conditions but maintain a consistent set of host-associated bacteria

    The copy numbers for 16S and ITS1 rRNA, and the sequencing depth for all samples are presented in Supplementary File 3 (qPCR data, Sequencing Rarefaction Curves). An average of 14,265.25 reads per housefly sample for the V4 16SrRNA and 16,149.4 reads per housefly sample for the ITS1 were retained after quality filtering. After quality filtering of the egg-laying substrate samples, an average of 10,371.75 reads were retained per sample for the V4 16SrRNA, and an average of 25,479.75 reads were retained per sample for the ITS1 region. The extracted DNA from newly emerged adult houseflies of the Spanish laboratory strain (12 samples in total, newly emerged adults, three replicates from four generations, strain SP100) returned a low copy number for the fungal ITS1 (qPCR data, Supplementary File 3) and a low number of acquired sequencing reads; they were therefore omitted from any further analysis of the fungal microbiota. In addition, the mitochondrial COI phylogeny showed that the Dutch wild-caught strain and the Dutch laboratory strain, which were sampled from the same locality at different times, are in close proximity and form a separate clade from the Spanish lab strain phylotypes (Supplementary File 2).The housefly microbiota alpha-diversity is determined by sampling environmentAbsolute richness (number of ASVs), Shannon index, and Phylogenetic diversity for all housefly strains and developmental stages are shown in Fig. 1. The highest bacterial alpha diversity was observed for the wild-caught housefly population GK0. Strain was an important factor for separating Shannon biodiversity levels both for newly emerged (F = 4.37, P  More

  • in

    Microbiota mediated plasticity promotes thermal adaptation in the sea anemone Nematostella vectensis

    Huxley, J. Evolution. The Modern Synthesis (Allen & Unwin, 1942).Bay, R. A. & Palumbi, S. R. Rapid acclimation ability mediated by transcriptome changes in reef-building corals. Genome Biol. Evol. 7, 1602–1612 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014).CAS 
    PubMed 

    Google Scholar 
    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).PubMed 

    Google Scholar 
    Fraune, S., ForĂȘt, S. & Reitzel, A. M. Using Nematostella vectensis to study the interactions between genome, epigenome, and bacteria in a changing environment. Front. Mar. Sci. 3, 1–8 (2016).
    Google Scholar 
    Kolodny, O. & Schulenburg, H. Opinion piece Microbiome-mediated plasticity directs host evolution along several distinct time scales. Phil. Trans. R. Soc. B 375, 20190589 (2020).Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073 (2006).CAS 
    PubMed 

    Google Scholar 
    Webster, N. S. & Reusch, T. B. H. Microbial contributions to the persistence of coral reefs. ISME J. 11, 2167–2174 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Totton, A. K. The British sea anemones. Nature 135, 977–978 (1935).
    Google Scholar 
    Hand, C. & Uhlinger, K. R. The unique, widely distributed, estuarine sea anemone, Nematostella vectensis Stephenson: a review, new facts, and questions. Estuaries 17, 501–501 (1994).
    Google Scholar 
    Darling, J. A., Reitzel, A. M. & Finnerty, J. R. Regional population structure of a widely introduced estuarine invertebrate: Nematostella vectensis Stephenson in New England. Mol. Ecol. 13, 2969–2981 (2004).CAS 
    PubMed 

    Google Scholar 
    Darling, J. A. et al. Rising starlet: the starlet sea anemone, Nematostella vectensis. BioEssays 27, 211–221 (2005).CAS 
    PubMed 

    Google Scholar 
    Hand, C. & Uhlinger, K. R. The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol. Bull. 182, 169–176 (1992).CAS 
    PubMed 

    Google Scholar 
    Pearson, C. V. M., Rogers, A. D. & Sheader, M. The genetic structure of the rare lagoonal sea anemone, Nematostella vectensis Stephenson (Cnidaria; Anthozoa) in the United Kingdom based on RAPD analysis. Mol. Ecol. 11, 2285–2293 (2002).CAS 
    PubMed 

    Google Scholar 
    Reitzel, A. M., Darling, J. A., Sullivan, J. C. & Finnerty, J. R. Global population genetic structure of the starlet anemone Nematostella vectensis: multiple introductions and implications for conservation policy. Biol. Invasions 10, 1197–1213 (2008).
    Google Scholar 
    Stefanik, D. J., Friedman, L. E. & Finnerty, J. R. Collecting, rearing, spawning and inducing regeneration of the starlet sea anemone, Nematostella vectensis. Nat. Protoc. 8, 916–923 (2013).PubMed 

    Google Scholar 
    Fritzenwanker, J. H. & Technau, U. Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212, 99–103 (2002).PubMed 

    Google Scholar 
    Mortzfeld, B. M. et al. Response of bacterial colonization in Nematostella vectensis to development, environment, and biogeography. Environ. Microbiol. 18, 1764–1781 (2016).PubMed 

    Google Scholar 
    Baldassarre, L. et al. Contribution of maternal and paternal transmission to bacterial colonization in Nematostella vectensis. Front. Microbiol. 12, 2892 (2021).
    Google Scholar 
    Domin, H. et al. Predicted bacterial interactions affect in vivo microbial colonization dynamics in Nematostella. Front. Microbiol. 9, 728 (2018).Guest, J. J. R. et al. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7, e33353–e33353 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Puisay, A., Pilon, R., Goiran, C. & HĂ©douin, L. Thermal resistances and acclimation potential during coral larval ontogeny in Acropora pulchra. Mar. Environ. Res. 135, 1–10 (2018).CAS 
    PubMed 

    Google Scholar 
    Van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl Acad. Sci. USA 112, 2313 (2015).
    Google Scholar 
    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Change 7, 627–636 (2017).
    Google Scholar 
    Yu, Xiaopeng et al. Thermal acclimation increases heat tolerance of the scleractinian coral Acropora pruinosa,. Sci. Total Environ. 733, 139319–139319 (2020).CAS 
    PubMed 

    Google Scholar 
    Jury, C. P. & Toonen, R. J. Adaptive responses and local stressor mitigation drive coral resilience in warmer, more acidic oceans. Proc. R. Soc. B Biol. Sci. 286, 20190614–20190614 (2019).
    Google Scholar 
    Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 5 (2019).
    Google Scholar 
    Thomas, L. et al. Mechanisms of thermal tolerance in reef-building corals across a fine-grained environmental mosaic: lessons from Ofu,. Am. Samoa. Front. Mar. Sci. 4, 434 (2018).
    Google Scholar 
    Oliver, T. A. & Palumbi, S. R. Many corals host thermally resistant symbionts in high-temperature habitat. Coral Reefs 30, 241–250 (2011).
    Google Scholar 
    Kenkel, C. D. & Matz, M. V. Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nat. Ecol. Evol. 1, 14 (2017).Barker, V. Exceptional thermal tolerance of coral reefs in American Samoa a review. Curr. Clim. Change Rep. 4, 427 (2018).
    Google Scholar 
    Bourne, D., Iida, Y., Uthicke, S. & Smith-Keune, C. Changes in coral-associated microbial communities during a bleaching event. ISME J. 2, 350–63 (2008).CAS 
    PubMed 

    Google Scholar 
    Carrier, T. J. & Reitzel, A. M. The hologenome across environments and the implications of a host-associated microbial repertoire. Front. Microbiol. 8, 802 (2017).Koren, O. & Rosenberg, E. Bacteria associated with mucus and tissues of the coral Oculina patagonica in summer and winter. Appl. Environ. Microbiol. 72, 5254–5259 (2006).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Littman, R., Willis, B. L. & Bourne, D. G. Metagenomic analysis of the coral holobiont during a natural bleaching event on the Great Barrier Reef. Environ. Microbiol. Rep. 3, 651–60 (2011).CAS 
    PubMed 

    Google Scholar 
    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213–14213 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thurber, R. V. et al. Metagenomic analysis of stressed coral holobionts. Environ. Microbiol. 11, 2148–2163 (2009).CAS 

    Google Scholar 
    van Oppen, M. J. H. & Blackall, L. L. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17, 557–567 (2019).PubMed 

    Google Scholar 
    Moran, N. A. & Yun, Y. Experimental replacement of an obligate insect symbiont. Proc. Natl Acad. Sci. USA 112, 2093–2096 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ainsworth, T. D. T. et al. The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J. 9, 2261–2274 (2015).CAS 

    Google Scholar 
    Hester, E. R., Barott, K. L., Nulton, J., Vermeij, M. J. A. & Rohwer, F. L. Stable and sporadic symbiotic communities of coral and algal holobionts. ISME J. 10, 1157–1169 (2016).CAS 
    PubMed 

    Google Scholar 
    Bourne, D. G., Morrow, K. M. & Webster, N. S. Insights into the coral microbiome: underpinning the health and resilience of reef ecosystems. Annu. Rev. Microbiol. 70, 340 (2016).
    Google Scholar 
    Pollock, F. J. et al. Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals. R. Soc. Open Sci. 6, 31312497 (2019).Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735 (2008).CAS 
    PubMed 

    Google Scholar 
    Elena, S. F. & Lenski, R. E. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4, 457–469 (2003).CAS 
    PubMed 

    Google Scholar 
    Hehemann, J. H. et al. Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464, 908–912 (2010).CAS 
    PubMed 

    Google Scholar 
    Bourne, D. G. Microbiological assessment of a disease outbreak on corals from Magnetic Island (Great Barrier Reef, Australia). Coral Reefs 24, 304–312 (2005).
    Google Scholar 
    Leach, W. B., Carrier, T. J. & Reitzel, A. M. Diel patterning in the bacterial community associated with the sea anemone Nematostella vectensis. Ecol. Evol. 9, 9935–9947 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Pootakham, W. et al. Heat-induced shift in coral microbiome reveals several members of the Rhodobacteraceae family as indicator species for thermal stress in Porites lutea. MicrobiologyOpen 8, e935 (2019).Webster, N. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6, 19324 (2016).Van, K. L., Ae, A., Schupp, P. & Slattery, M. The distribution of dimethylsulfoniopropionate in tropical Pacific coral reef invertebrates. Coral Reefs 25, 321–327 (2006).
    Google Scholar 
    Rypien, K. L., Ward, J. R. & Azam, F. Antagonistic interactions among coral-associated bacteria. Environ. Microbiol. 12, 28–39 (2010).CAS 
    PubMed 

    Google Scholar 
    Blazejak, A., ErsĂ©us, C., Amann, R. & Dubilier, N. Coexistence of bacterial sulfide oxidizers, sulfate reducers, and spirochetes in a gutless worm (oligochaeta) from the Peru margin. Appl. Environ. Microbiol. 71, 1553–1561 (2005).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dubilier, N. et al. Phylogenetic diversity of bacterial endosymbionts in the gutless marine oligochete Olavius loisae (Annelida). Mar. Ecol. Prog. Ser. 178, 271–280 (1999).
    Google Scholar 
    Rincón-Rosales, R., Lloret, L., Ponce, E. & Martínez-Romero, E. Erratum: Rhizobia with different symbiotic efficiencies nodulate Acaciella angustissima in Mexico, including Sinorhizobium chiapanecum sp. nov. which has common symbiotic genes with Sinorhizobium mexicanum (FEMS Microbiology Ecology (2009) 67 (103-117)). FEMS Microbiol. Ecol. 68, 255–255 (2009).
    Google Scholar 
    Rosenberg, E. & DeLong, E. F., Stackebrandt, E., Lory, S., Thompson, F. The Prokaryotes—Prokaryotic Biology and Symbiotic Associations. (Springer, 2013).Kimura, H., Higashide, Y. & Naganuma, T. Endosymbiotic microflora of the Vestimentiferan Tubeworm (Lamellibrachia sp.) from a Bathyal Cold Seep. Mar. Biotechnol. 5, 593–603 (2003).CAS 

    Google Scholar 
    Melillo, A. A., Bakshi, C. S. & Melendez, J. A. Francisella tularensis antioxidants harness reactive oxygen species to restrict macrophage signaling and cytokine production. J. Biol. Chem. 285, 27553–27560 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rabadi, S. M. et al. Antioxidant defenses of Francisella tularensis modulate macrophage function and production of proinflammatory cytokines. J. Biol. Chem. 291, 5009–5021 (2016).CAS 
    PubMed 

    Google Scholar 
    McBride, M. J. in The Prokaryotes: Other Major Lineages of Bacteria and The Archaea. Vol. 9783642389542, 643–676 (Springer-Verlag Berlin Heidelberg, 2014).Augustin, R., Fraune, S. & Bosch, T. C. G. How Hydra senses and destroys microbes. Semin. Immunol. 22, 54–58 (2010).CAS 
    PubMed 

    Google Scholar 
    Augustin, R. et al. A secreted antibacterial neuropeptide shapes the microbiome of Hydra. Nat. Commun. 8, 698 (2017).Franzenburg, S. et al. Distinct antimicrobial peptide expression determines host species-specific bacterial associations. Proc. Natl Acad. Sci. USA 110, E3730–E3738 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Fraune, S., Abe, Y. & Bosch, T. C. G. G. Disturbing epithelial homeostasis in the metazoan Hydra leads to drastic changes in associated microbiota. Environ. Microbiol. 11, 2361–9 (2009).CAS 
    PubMed 

    Google Scholar 
    Brennan, J. J. et al. Sea anemone model has a single Toll-like receptor that can function in pathogen detection, NF-ÎșB signal transduction, and development. Proc. Natl Acad. Sci. USA 114, E10122–E10131 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sullivan, J. C. et al. Two alleles of NF-ÎșB in the sea anemone Nematostella vectensis are widely dispersed in nature and encode proteins with distinct activities. PLoS ONE 4, e7311 (2009).Wolenski, F. S. et al. Characterization of the core elements of the NF-B signaling pathway of the sea anemone Nematostella vectensis. Mol. Cell. Biol. 31, 1076–1087 (2011).CAS 
    PubMed 

    Google Scholar 
    Gáliková, M., Klepsatel, P., Senti, G. & Flatt, T. Steroid hormone regulation of C. elegans and Drosophila aging and life history. Exp. Gerontol. 46, 141–147 (2011).PubMed 

    Google Scholar 
    Taubenheim, J., Kortmann, C. & Fraune, S. Function and evolution of nuclear receptors in environmental-dependent postembryonic development. Front. Cell Dev. Biol. 9, 653792 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Becker, P. B. & Workman, J. L. Nucleosome remodeling and epigenetics. Cold Spring Harb. Perspect. Biol. 5, a017905–a017905 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Barno, A. R., Villela, H. D. M., Aranda, M., Thomas, T. & Peixoto, R. S. Host under epigenetic control: a novel perspective on the interaction between microorganisms and corals. BioEssays 43, 2100068.Reitzel, A. M. et al. Physiological and developmental responses to temperature by the sea anemone Nematostella vectensis. Mar. Ecol. Prog. Ser. 484, 115–130 (2013).
    Google Scholar 
    Chua, C. M., Leggat, W., Moya, A. & Baird, A. H. Temperature affects the early life history stages of corals more than near future ocean acidification. Mar. Ecol. Prog. Ser. 475, 85–92 (2013).
    Google Scholar 
    Ericson, J. A. et al. Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri. Polar Biol. 35, 1027–1034 (2012).
    Google Scholar 
    Sheppard Brennand, H., Soars, N., Dworjanyn, S. A., Davis, A. R. & Byrne, M. Impact of ocean warming and ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. PLoS ONE 5, e11372 (2010).Bernal, M. A. et al. Phenotypic and molecular consequences of stepwise temperature increase across generations in a coral reef fish. Mol. Ecol. 27, 4516–4528 (2018).CAS 
    PubMed 

    Google Scholar 
    Clark, M. S. et al. Molecular mechanisms underpinning transgenerational plasticity in the green sea urchin Psammechinus miliaris. Sci. Rep. 9, 1–12 (2019).
    Google Scholar 
    Donelson, J. et al. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change 2, 30–32 (2012).
    Google Scholar 
    Miller, G. M., Watson, S. A., Donelson, J. M., McCormick, M. I. & Munday, P. L. Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nat. Clim. Change 2, 858–861 (2012).CAS 

    Google Scholar 
    Munday, P. L. Transgenerational acclimation of fishes to climate change and ocean acidification. F1000Prime Rep. 6, 99–99 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Ryu, T. et al. An epigenetic signature for within-generational plasticity of a reef fish to ocean warming. Front. Mar. Sci. 7, 284 (2020).Veilleux, H. et al. Molecular processes of transgenerational acclimation to a warming ocean. Nat. Clim. Change 5, 1074–1078 (2015).CAS 

    Google Scholar 
    Zhao, C. et al. Transgenerational effects of ocean warming on the sea urchin Strongylocentrotus intermedius. Ecotoxicol. Environ. Saf. 151, 212–219 (2018).CAS 
    PubMed 

    Google Scholar 
    Eirin-Lopez, J. M. & Putnam, H. M. Marine Environmental Epigenetics. Annu. Rev. Mar. Sci. 11, 335–368 (2019).
    Google Scholar 
    Fallet, M., Luquet, E., David, P. & Cosseau, C. Epigenetic inheritance and intergenerational effects in mollusks. Gene 729, 144166–144166 (2020).CAS 
    PubMed 

    Google Scholar 
    Putnam, H. M. & Gates, R. D. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J. Exp. Biol. 218, 2365–2372 (2015).PubMed 

    Google Scholar 
    Daxinger, L. & Whitelaw, E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 20, 1623–1628 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ptashne, M. Epigenetics: core misconcept. Proc. Natl Acad. Sci. USA 110, 7101–7103 (2013).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rivera, H. E., Chen, C.-Y., Gibson, M. C. & Tarrant, A. M. Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis. J. Exp. Biol. 224, jeb236745 (2021).Hirose, E. & Fukuda, T. Vertical transmission of photosymbionts in the colonial ascidian Didemnum molle: The larval tunic prevents symbionts from attaching to the anterior part of larvae. Zool. Sci. 23, 669–674 (2006).
    Google Scholar 
    Padilla-Gamiño, J. L., Pochon, X., Bird, C., Concepcion, G. T. & Gates, R. D. From parent to gamete: vertical transmission of Symbiodinium (Dinophyceae) ITS2 sequence assemblages in the reef building coral Montipora capitata. PLoS ONE 7, e38440–e38440 (2012).PubMed 
    PubMed Central 

    Google Scholar 
    Sharp, K. H., Eam, B., John Faulkner, D. & Haygood, M. G. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl. Environ. Microbiol. 73, 622–629 (2007).CAS 
    PubMed 

    Google Scholar 
    Sipkema, D. et al. Similar sponge-associated bacteria can be acquired via both vertical and horizontal transmission. Environ. Microbiol. 17, 3807–3821 (2015).CAS 
    PubMed 

    Google Scholar 
    Apprill, A., Marlow, H. Q., Martindale, M. Q. & RappĂ©, M. S. The onset of microbial associations in the coral Pocillopora meandrina. ISME J. 3, 685–699 (2009).PubMed 

    Google Scholar 
    Sharp, K. H., Distel, D. & Paul, V. J. Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides. ISME J. 6, 790–801 (2012).CAS 
    PubMed 

    Google Scholar 
    Lesser, M. P., Stat, M. & Gates, R. D. The endosymbiotic dinoflagellates (Symbiodinium sp.) of corals are parasites and mutualists. Coral Reefs 32, 603–611 (2013).
    Google Scholar 
    Ceh, J., Raina, J. B., Soo, R. M., van Keulen, M. & Bourne, D. G. Coral-bacterial communities before and after a coral mass spawning event on Ningaloo Reef. PLoS ONE 7, e36920 (2012).Ricardo, G. F., Jones, R. J., Negri, A. P. & Stocker, R. That sinking feeling: suspended sediments can prevent the ascent of coral egg bundles. Sci. Rep. 6, 21567 (2016).Leite, D. C. A. D. et al. Broadcast spawning coral Mussismilia Hispida can vertically transfer its associated bacterial core. Front. Microbiol. 8, 176–176 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Epstein, H. E. et al. Microbiome engineering: enhancing climate resilience in corals. Front. Ecol. Environ. 17, 108 (2019).
    Google Scholar 
    Peixoto, R. S. et al. Beneficial microorganisms for corals (BMC) Proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 341 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. H. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Change Biol. 23, 4675–4688 (2017).
    Google Scholar 
    Damjanovic, K., Blackall, L. L., Webster, N. S. & van Oppen, M. J. H. H. The contribution of microbial biotechnology to mitigating coral reef degradation. Microb. Biotechnol. 10, 1236–1243 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Damjanovic, K., Van Oppen, M. J. H., MenĂ©ndez, P. & Blackall, L. L. Experimental inoculation of coral recruits with marine bacteria indicates scope for microbiome manipulation in Acropora tenuis and Platygyra daedalea. Front. Microbiol. 10, 1702 (2019).Rosado, P. M. et al. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13, 921–936 (2019).CAS 
    PubMed 

    Google Scholar 
    Fraune, S. et al. Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J. 9, 1543–1556 (2015).CAS 
    PubMed 

    Google Scholar 
    Fadrosh, D. W. et al. An improved dual-indexing approach for multiplexed 16 S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Rausch, P. et al. Analysis of factors contributing to variation in the C57BL/6 J fecal microbiota across German animal facilities. Int. J. Med. Microbiol. 306, 343–355 (2016).PubMed 

    Google Scholar 
    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439–1237439 (2013).PubMed 
    PubMed Central 

    Google Scholar 
    Segata, N. et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60–R60 (2011).PubMed 
    PubMed Central 

    Google Scholar 
    Andrews, S. FastQC: A Quality Control Tool for High Throughput Sequence Data [Online]. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (2010).Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat. Biotechnol. 33, 290–295 (2015).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shao, M. & Kingsford, C. accurate assembly of transcripts through phase-preserving graph decomposition. Nat. Biotechnol. 35, 1167–1169 (2017).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Niknafs, Y. S., Pandian, B., Iyer, H. K., Chinnaiyan, A. M. & Iyer, M. K. TACO produces robust multisample transcriptome assemblies from RNA-seq. Nat. Methods 14, 68–70 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Pertea, M. & Pertea, G. GFF Utilities: GffRead and GffCompare. F1000Research 9, 304–304 (2020).
    Google Scholar 
    Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38, 4647–4654 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).CAS 
    PubMed 

    Google Scholar 
    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550–550 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Law, C. W., Chen, Y., Shi, W. & Smyth, G. K. Voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29–R29 (2014).PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    Rapid Eocene diversification of spiny plants in subtropical woodlands of central Tibet

    Reich, P. B. et al. The evolution of plant functional variation: traits, spectra, and strategies. Int. J. Plant Sci. 164, S143–S164 (2003).
    Google Scholar 
    Cornelissen, J. H. C. et al. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust. J. Bot. 51, 335–380 (2003).
    Google Scholar 
    Liu, X. J. & Ma, K. P. Plant functional traits concepts, applications and future directions. Sci. Sin. Vitae 45, 325–339 (2015).
    Google Scholar 
    Diaz, S., Cabido, M. & Casanoves, F. Plant functional traits and environmental filters at a regional scale. J. Veg. Sci. 9, 113–122 (1998).
    Google Scholar 
    Kraft, N. J. B., Godoy, O. & Levine, J. M. Plant functional traits and the multidimensional nature of species coexistence. Proc. Natl Acad. Sci. USA 112, 797–802 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Barton, K. E. Tougher and thornier: general patterns in the induction of physical defence traits. Func. Ecol. 30, 181–187 (2016).
    Google Scholar 
    Adler, P. B., Fajardo, A., Kleinhesselink, A. R. & Kraft, N. J. B. Trait-based tests of coexistence mechanisms. Ecol. Lett. 16, 1294–1306 (2013).PubMed 

    Google Scholar 
    Wright, S. J. et al. Functional traits and the growth–mortality trade-off in tropical trees. Ecology 91, 3664–3674 (2010).PubMed 

    Google Scholar 
    Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Ruiz-Jaen, M. C. & Potvin, C. Can we predict carbon stocks in tropical ecosystems from tree diversity? Comparing species and functional diversity in a plantation and a natural forest. New Phytol. 189, 978–987 (2011).PubMed 

    Google Scholar 
    Grubb, P. J. A positive distrust in simplicity-lessons from plant defences and from competition among plants and among animals. J. Ecol. 80, 585–610 (1992).
    Google Scholar 
    Hanley, M. E., Lamont, B. B., Fairbanks, M. M. & Rafferty, C. M. Plant structural traits and their role in anti-herbivore defence. Perspect. Plant Ecol. 8, 157–178 (2007).
    Google Scholar 
    Burns, K. C. Spinescence in the New Zealand flora: parallels with Australia. N. Z. J. Bot. 54, 273–289 (2016).
    Google Scholar 
    Goheen, J. R., Young, T. P., Keesing, F. & Palmer, T. M. Consequences of herbivory by native ungulates for the reproduction of a savanna tree. J. Ecol. 95, 129–138 (2007).
    Google Scholar 
    Goldel, B., Kissling, W. D. & Svenning, J.-C. Geographical variation and environmental correlates of functional trait distributions in palms (Arecaceae) across the New World. Bot. J. Linn. Soc. 179, 602–617 (2015).
    Google Scholar 
    Alves-Silva, E. & Del-Claro, K. Herbivory causes increases in leaf spinescence and fluctuating asymmetry as a mechanism of delayed induced resistance in a tropical savanna tree. Plant Ecol. Evol. 149, 73–80 (2016).
    Google Scholar 
    Cooper, S. M. & Ginnett, T. F. Spines protect plants against browsing by small climbing mammals. Oecologia 113, 219–221 (1998).ADS 
    PubMed 

    Google Scholar 
    Charles-Dominique, T. et al. Spiny plants, mammal browsers, and the origin of African savannas. Proc. Natl Acad. Sci. USA 113, E5572–E5579 (2016).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ratnam, J., Tomlinson, K. W., Rasquinha, D. N. & Sankaran, M. Savannahs of Asia: antiquity, biogeography, and an uncertain future. Philos. Trans. R. Soc. B. 371, 20150305 (2016).
    Google Scholar 
    Scholes, R. & Archer, S. Tree-grass interactions in savannas. Annu. Rev. Ecol. Syst. 28, 517–544 (1997).
    Google Scholar 
    Cerling, T. E. Development of grasslands and savannas in East Africa during the Neogene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 97, 241–247 (1992).
    Google Scholar 
    Brown, R. W. Additions to the flora of the Green River formation. U. S. Geol. Surv. Prof. Paper, U. S. Gov. Print. Off. 154-J, 279–292 (1929).Manchester, S. Oligocene fossil plants of the John Day Formation, Oregon. Or. Geol. 49, 115d–127d (1987).
    Google Scholar 
    Meyer, H. W. & Manchester, S. R. Oligocene Bridge Creek flora of the John Day Formation, Oregon (Univ. California Press, 1997).Lancucka-Srodoniowa, M. Tortonian flora from the “Gdow Bay” in the south of Poland. Acta Palaeobot. 7, 1–134 (1966).
    Google Scholar 
    Yuan, J. et al. Rapid drift of the Tethyan Himalaya terrane before two-stage India-Asia collision. Natl Sci. Rev. 8, nwaa173 (2021).PubMed 

    Google Scholar 
    Spicer, R. A. et al. Why the ‘Uplift of the Tibetan Plateau’is a myth. Natl Sci. Rev. 8, nwaa091 (2021).PubMed 

    Google Scholar 
    Spicer, R. A. Tibet, the Himalaya, Asian monsoons and biodiversity–In what ways are they related? Plant Divers. 39, 233–244 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    DeCelles, P. G., Kapp, P., Gehrels, G. E. & Ding, L. Paleocene-Eocene foreland basin evolution in the Himalaya of southern Tibet and Nepal: implications for the age of initial India-Asia collision. Tectonics 33, 824–849 (2014).ADS 

    Google Scholar 
    Royden, L. H., Burchfiel, B. C. & van der Hilst, R. D. The geological evolution of the Tibetan Plateau. Science 321, 1054–1058 (2008).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Deng, T., Wu, F. X., Zhou, Z. K. & Su, T. Tibetan Plateau: an evolutionary junction for the history of modern biodiversity. Sci. China Earth Sci. 63, 172–187 (2020).ADS 

    Google Scholar 
    Favre, A. et al. The role of the uplift of the Qinghai‐Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. 90, 236–253 (2015).PubMed 

    Google Scholar 
    Su, T. et al. A Middle Eocene lowland humid subtropical “Shangri-La” ecosystem in central Tibet. Proc. Natl Acad. Sci. USA 117, 32989–32995 (2020).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Scientific Expedition Team to the Qinghai-Xizang Plateau. Vegetation of Xizang (Tibet) (Sci. Press, 1988).Liu. X. H. Paleoelevation History and Evolution of the Cenozoic Lunpola basin, Central Tibet. Doctoral thesis (Institute of Tibetan Plateau Research, Chinese Academy of Sciences, 2018).Xiong, Z. Y. et al. The rise and demise of the Paleogene Central Tibetan Valley. Sci. Adv. 8, eabj0944 (2022).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Reichgelt, T., West, C. K. & Greenwood, D. R. The relation between global palm distribution and climate. Sci. Rep. 8, 4721 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Farnsworth, A. et al. Paleoclimate model-derived thermal lapse rates: towards increasing precision in paleoaltimetry studies. Earth Planet. Sci. Lett. 564, 116903 (2021).CAS 

    Google Scholar 
    Spicer, R. A. et al. Why do foliar physiognomic climate estimates sometimes differ from those observed? Insights from taphonomic information loss and a CLAMP case study from the Ganges Delta. Palaeogeogr. Palaeoclimatol. Palaeoecol. 302, 381–395 (2011).
    Google Scholar 
    Walter, H. Vegetation of the Earth and Ecological Systems of the Geo-biosphere (Springer Berlin Heidelb., 1973).Burley, J. Encyclopedia of Forest Sciences (Acad. Press, 2004).Deng, T. et al. A mammalian fossil from the Dingqing Formation in the Lunpola Basin, northern Tibet, and its relevance to age and paleo-altimetry. Sci. Bull. 57, 261–269 (2012).CAS 

    Google Scholar 
    Ma, P. F. et al. Late Oligocene-early Miocene evolution of the Lunpola Basin, central Tibetan Plateau, evidences from successive lacustrine records. Gondwana Res. 48, 224–236 (2017).ADS 

    Google Scholar 
    Hempson, G. P., Archibald, S. & Bond, W. J. A continent-wide assessment of the form and intensity of large mammal herbivory in Africa. Science 350, 1056–1061 (2015).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Spicer, R. A. The formation and interpretation of plant fossil assemblages. Adv. Bot. Res. 16, 95–191 (1989).
    Google Scholar 
    Gibson, D. J. Grasses and Grassland Ecology (Oxford Univ. Press, 2009).Eltringham, S. K. The Hippos: Natural History and Conservation (Princeton Univ. Press, 1999).Jiang, H. et al. Oligocene Koelreuteria (Sapindaceae) from the Lunpola Basin in central Tibet and its implication for early diversification of the genus. J. Asian Earth Sci. 175, 99–108 (2019).ADS 

    Google Scholar 
    Liu, J. et al. Biotic interchange through lowlands of Tibetan Plateau suture zones during Paleogene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 524, 33–40 (2019).
    Google Scholar 
    Jia, L. B. et al. First fossil record of Cedrelospermum (Ulmaceae) from the Qinghai-Tibetan Plateau: implications for morphological evolution and biogeography. J. Syst. Evol. 57, 94–104 (2019).
    Google Scholar 
    Su, T. et al. No high Tibetan Plateau until the Neogene. Sci. Adv. 5, eaav2189 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zhang, Y. L., Li, B. Y. & Zheng, D. A discussion on the boundary and area of the Tibetan Plateau in China. Geol. Res. 21, 1–8 (2002).
    Google Scholar 
    Yao, T. D. et al. From Tibetan Plateau to Third Pole and Pan-Third Pole. Bull. Chin. Acad. Sci. 32, 924–931 (2017).
    Google Scholar 
    Spicer, R. A., Farnsworth, A. & Su, T. Cenozoic topography, monsoons and biodiversity conservation within the Tibetan Region: an evolving story. Plant Divers. 42, 229–254 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Liu, X. H., Xu, Q. & Ding, L. Differential surface uplift: Cenozoic paleoelevation history of the Tibetan Plateau. Sci. China Earth Sci. 59, 2105–2120 (2016).ADS 
    CAS 

    Google Scholar 
    Ding, L., Li, Z. Y. & Song, P. P. Core fragments of Tibetan Plateau from Gondwanaland united in Northern Hemisphere. Bull. Chin. Acad. Sci. 32, 945–950 (2017).
    Google Scholar 
    Deng, T. & Ding, L. Paleoaltimetry reconstructions of the Tibetan Plateau: progress and contradictions. Natl Sci. Rev. 2, 417–437 (2015).CAS 

    Google Scholar 
    Li, S. F. et al. Orographic evolution of northern Tibet shaped vegetation and plant diversity in eastern Asia. Sci. Adv. 7, eabc7741 (2021).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ding, L. et al. The Andean-type Gangdese Mountains: Paleoelevation record from the Paleocene–Eocene Linzhou Basin. Earth Planet. Sci. Lett. 392, 250–264 (2014).ADS 
    CAS 

    Google Scholar 
    Deng, T. et al. Review: implications of vertebrate fossils for paleo-elevations of the Tibetan Plateau. Glob. Planet. Change 174, 58–69 (2019).ADS 

    Google Scholar 
    Westerhold, T. et al. An astronomically dated record of Earth’s climate and its predictability over the last 66 million years. Science 369, 1383–1387 (2020).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Nemani, R. R. et al. Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science 300, 1560–1563 (2003).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Hopkins, W. G. Introduction to Plant Physiology (John Wiley & Sons, 1999).Sun, J. M., Liu, W. G., Liu, Z. H. & Fu, B. H. Effects of the uplift of the Tibetan Plateau and retreat of Neotethys ocean on the stepwise aridification of mid-latitude Asian interior. Bull. Chin. Acad. Sci. 32, 951–958 (2017).
    Google Scholar 
    Zong, G. F. Cenezoic Mammals and Environment of Hengduan Mountains Region (China Ocean Press, 1996).Deng, T. et al. An Oligocene giant rhino provides insights into Paraceratherium evolution. Commun. Biol. 4, 639 (2021).PubMed 
    PubMed Central 

    Google Scholar 
    Young, T. P., Stanton, M. L. & Christian, C. E. Effects of natural and simulated herbivory on spine lengths of Acacia drepanolobium in Kenya. Oikos 101, 171–179 (2003).
    Google Scholar 
    Karban, R. & Myers, J. H. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20, 331–348 (1989).
    Google Scholar 
    Huntly, N. Herbivores and the dynamics of communities and ecosystems. Annu. Rev. Ecol. Syst. 22, 477–503 (1991).
    Google Scholar 
    Asner, G. P. et al. Large-scale impacts of herbivores on the structural diversity of African savannas. Proc. Natl Acad. Sci. USA 106, 4947–4952 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sankaran, M., Augustine, D. J. & Ratnam, J. Native ungulates of diverse body sizes collectively regulate long‐term woody plant demography and structure of a semi‐arid savanna. J. Ecol. 101, 1389–1399 (2013).
    Google Scholar 
    Staver, A. C. & Bond, W. J. Is there a ‘browse trap’? Dynamics of herbivore impacts on trees and grasses in an African savanna. J. Ecol. 102, 595–602 (2014).
    Google Scholar 
    Bakker, E. S. et al. Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation. Proc. Natl Acad. Sci. USA 113, 847–855 (2016).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Spicer, R. A. et al. The topographic evolution of the Tibetan Region as revealed by palaeontology. Palaeobio. Palaeoenv. 101, 213–243 (2021).
    Google Scholar 
    Rowley, D. B. & Currie, B. S. Palaeo-altimetry of the late Eocene to Miocene Lunpola basin, central Tibet. Nature 439, 677–681 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Sun, J. M. et al. Palynological evidence for the latest Oligocene-early Miocene paleoelevation estimate in the Lunpola Basin, central Tibet. Palaeogeogr. Palaeoclimatol. Palaeoecol. 399, 21–30 (2014).
    Google Scholar 
    DeCelles, P. G., Kapp, P., Ding, L. & Gehrels, G. E. Late Cretaceous to middle Tertiary basin evolution in the central Tibetan Plateau: Changing environments in response to tectonic partitioning, aridification, and regional elevation gain. Geol. Soc. Am. Bull. 119, 654–680 (2007).ADS 

    Google Scholar 
    Tang, H. et al. Extinct genus Lagokarpos reveals a biogeographic connection between Tibet and other regions in the Northern Hemisphere during the Paleogene. J. Syst. Evol. 57, 670–677 (2019).
    Google Scholar 
    Wang, T. X. et al. Fossil fruits of Illigera (Hernandiaceae) from the Eocene of central Tibetan Plateau. J. Syst. Evol. 59, 1276–1286 (2021).
    Google Scholar 
    Del Rio, C. et al. Asclepiadospermum gen. nov., the earliest fossil record of Asclepiadoideae (Apocynaceae) from the early Eocene of central Qinghai-Tibetan Plateau, and its biogeographic implications. Am. J. Bot. 107, 126–138 (2020).PubMed 

    Google Scholar 
    Xu, Z. Y. The Tertiary and its petroleum potential in the Lunpola Basin, Tibet. Oil Gas. Geol. 1, 153–158 (1980).
    Google Scholar 
    Zhang, K. X. et al. Paleogene-Neogene stratigraphic realm and sedimentary sequence of the Qinghai-Tibet Plateau and their response to uplift of the plateau. Sci. China Earth Sci. 53, 1271–1294 (2010).ADS 

    Google Scholar 
    Wu, Y. F. & Chen, Y. Y. Fossil cyprinid fishes from the late Tertiary of north Xizang, China. Vertebrata Palasiat. 18, 15–20 (1980).
    Google Scholar 
    Wu, F. X., Miao, D. S., Chang, M. M., Shi, G. L. & Wang, N. Fossil climbing perch and associated plant megafossils indicate a warm and wet central Tibet during the late Oligocene. Sci. Rep. 7, 878 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cai, C. Y., Huang, D. Y., Wu, F. X., Zhao, M. & Wang, N. Tertiary water striders (Hemiptera, Gerromorpha, Gerridae) from the central Tibetan Plateau and their palaeobiogeographic implications. J. Asian Earth Sci. 175, 121–127 (2017).ADS 

    Google Scholar 
    Low, S. L. et al. Oligocene Limnobiophyllum (Araceae) from the central Tibetan Plateau and its evolutionary and palaeoenvironmental implications. J. Syst. Palaeontol. 18, 415–431 (2020).
    Google Scholar 
    Bell, A. D. & Bryan, A. Plant Form: An Illustrated Guide to Flowering Plant Morphology (Timber Press, 2008).Zanne, A. E. et al. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89–92 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
    Google Scholar 
    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 35, 526–528 (2019).CAS 
    PubMed 

    Google Scholar 
    Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics. 24, 129–131 (2008).CAS 
    PubMed 

    Google Scholar 
    Maddison, W. P. Confounding asymmetries in evolutionary diversification and character change. Evolution 60, 1743–1746 (2006).PubMed 

    Google Scholar 
    Forest, C. E., Molnar, P. & Emanuel, K. A. Palaeoaltimetry from energy conservation principles. Nature 374, 347–350 (1995).ADS 
    CAS 

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

    Google Scholar 
    Gough, D. O. Solar interior structure and luminosity variations. Sol. Phys. 74, 21–34 (1981).ADS 
    CAS 

    Google Scholar 
    Foster, G. L., Royer, D. L. & Lunt, D. J. Future climate forcing potentially without precedent in the last 420 million years. Nat. Commun. 8, 14845 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Cox, P. M. Description of the “TRIFFID” Dynamic Global Vegetation Model. 1–16 (Met Office Hadley Centre, 2001).Cox, P., Huntingford, C. & Harding, R. A canopy conductance and photosynthesis model for use in a GCM land surface scheme. J. Hydrol. 212, 79–94 (1998).ADS 

    Google Scholar 
    McInerney, F. A., Strömberg, C. A. E. & White, J. W. C. The Neogene transition from C3 to C4 grasslands in North America stable carbon isotope ratios of fossil phytoliths. Paleobiology 37, 23–49 (2011).
    Google Scholar 
    Lu, H. Y. et al. Phytoliths as quantitative indicators for the reconstruction of past environmental conditions in China II: palaeoenvironmental reconstruction in the Loess Plateau. Quat. Sci. Rev. 25, 945–959 (2006).ADS 

    Google Scholar  More