Abstract
Climate change can lead to a mismatch between resource availability and key life history events. Without plasticity in reproductive traits, that mismatch can lower fitness and decrease population size. In birds, phenotypic plasticity is frequently reported as the main mechanism to track environmental changes, but evidence for plasticity in large mammals is scarce. Using long-term individual-based data, we quantified phenotypic plasticity in 394 parturition dates of 137 bighorn sheep ewes (average 2.9 per ewe, range 1–11 parturition dates) in response to environmental drivers. Over 26 years, we detected a population response to environmental drivers, as median parturition date advanced by 15 days. Our study area showed temporal trends in population density, precipitation in October–November and temperature in August–November. Increasing autumn precipitation was associated with later parturition. Increasing autumn temperature was associated with earlier parturition but the effect was weak. Analyses of the between- and within-individual components of weather, climate and density revealed an individual adjustment to autumn precipitation. We detected no plasticity in response to variation in temperature and density and no variation in plasticity (no I × E) in response to any determinants of parturition date. Our results suggest that the reproductive phenology of species with long and fixed gestation may respond more to environmental drivers in autumn than in spring.
Significance statement
Many organisms time reproductive events based on seasonal availability of food resources. Climate change, however, can affect the timing of food availability. Organisms can change the timing of reproduction over the short term through phenotypic plasticity. Little is known, however, about how much individual plasticity in reproductive timing exists in wild mammals. We examined phenotypic plasticity in parturition date in bighorn sheep in response to changes in autumn precipitation, autumn temperature, a global climate index and adult female density. Temporal trends in these variables over 26 years partly explained a 15-day advance in average parturition date. Individual ewes only appeared to show plasticity in response to autumn precipitation, suggesting some capacity to cope with rapid global environmental changes over the short term.
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References
Bailey LD, van de Pol M (2016) climwin: an R toolbox for climate window analysis. PLoS ONE 11:e0167980. https://doi.org/10.1371/journal.pone.0167980
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Both C, van Asch M, Bijlsma RG, van den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83. https://doi.org/10.1111/j.1365-2656.2008.01458.x
Bourret A, Bélisle M, Pelletier F, Garant D (2015) Multidimensional environmental influences on timing of breeding in a tree swallow population facing climate change. Evol Appl 8:933–944. https://doi.org/10.1111/eva.12315
Boutin S, Lane JE (2014) Climate change and mammals: evolutionary versus plastic responses. Evol Appl 7:29–41. https://doi.org/10.1111/eva.12121
Charmantier A, Gienapp P (2014) Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evol Appl 7:15–28. https://doi.org/10.1111/eva.12126
Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803. https://doi.org/10.1126/science.1157174
Clements MN, Clutton-Brock TH, Albon SD, Pemberton JM, Kruuk LEB (2011) Gestation length variation in a wild ungulate. Funct Ecol 25:691–703. https://doi.org/10.1111/j.1365-2435.2010.01812.x
Dantzer B, Newman AEM, Boonstra R, Palme R, Boutin S, Humphries MM, McAdam AG (2013) Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340:1215–1217. https://doi.org/10.1126/science.1235765
Douhard M, Pigeon G, Festa-Bianchet M, Coltman DW, Guillemette S, Pelletier F (2017) Environmental and evolutionary effects on horn growth of male bighorn sheep. Oikos 126:1031–1041. https://doi.org/10.1111/oik.03799
Feder C, Martin JGA, Festa-Bianchet M, Bérubé C, Jorgenson J (2008) Never too late? Consequences of late birthdate for mass and survival of bighorn lambs. Oecologia 156:773–781. https://doi.org/10.1007/s00442-008-1035-9
Festa-Bianchet M (1988a) Birthdate and survival in bighorn lambs (Ovis canadensis). J Zool 214:653–661. https://doi.org/10.1111/j.1469-7998.1988.tb03764.x
Festa-Bianchet M (1988b) Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36:1445–1454. https://doi.org/10.1016/S0003-3472(88)80215-X
Forchhammer MC, Clutton-Brock TH, Lindström J, Albon SD (2001) Climate and population density induce long-term cohort variation in a northern ungulate. J Anim Ecol 70:721–729. https://doi.org/10.1046/j.0021-8790.2001.00532.x
Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115:276–284. https://doi.org/10.1038/hdy.2014.92
Geist V (1971) Mountain sheep: a study in behavior and evolution. The University of Chicago Press, Chicago
Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P (2017) The evolution of phenotypic plasticity under global change. Sci Rep 7:17253. https://doi.org/10.1038/s41598-017-17554-0
Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178. https://doi.org/10.1111/j.1365-294X.2007.03413.x
Grosbois V, Gimenez O, Gaillard JM, Pradel R, Barbraud C, Clobert J, Møller AP, Weimerskirch H (2008) Assessing the impact of climate variation on survival in vertebrate populations. Biol Rev 83:357–399. https://doi.org/10.1111/j.1469-185X.2008.00047.x
Hogg JT (1984) Mating in bighorn sheep: multiple creative male strategies. Science 225:526–529
Hogg JT, Dunn SJ, Poissant J, Pelletier F, Byers JA (2017) Capital vs. income-dependent optimal birth date in two North American ungulates. Ecosphere 8:e01766. https://doi.org/10.1002/ecs2.1766
Jorgenson JT, Festa-Bianchet M, Lucherini M, Wishart WD (1993) Effects of body size, population density, and maternal characteristics on age at first reproduction in bighorn ewes. Can J Zool 71:2509–2517. https://doi.org/10.1139/z93-344
Lane JE, Kruuk LEB, Charmantier A, Murie JO, Dobson FS (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489:554–557. https://doi.org/10.1038/nature11335
Mantua NJ, Hare SR, Zhang Y, Wallace JM, Francis RC (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78:1069–1079. https://doi.org/10.1175/1520-0477(1997)078<1069:APICOW>2.0.CO;2
Martin JGA, Pelletier F (2011) Measuring growth patterns in the field: effects of sampling regime and methods on standardized estimates. Can J Zool 89:529–537. https://doi.org/10.1139/z11-018
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14. https://doi.org/10.1111/eva.12137
Moyes K, Nussey DH, Clements MN, Guinness FE, Morris A, Morris S, Pemberton JM, Kruuk LEB, Clutton-Brock TH (2011) Advancing breeding phenology in response to environmental change in a wild red deer population. Glob Change Biol 17:2455–2469. https://doi.org/10.1111/j.1365-2486.2010.02382.x
Mysterud A, Bonenfant C, Loe LE, Langvatn R, Yoccoz NG, Stenseth NC (2008) The timing of male reproductive effort relative to female ovulation in a capital breeder. J Anim Ecol 77:469–477. https://doi.org/10.1111/j.1365-2656.2008.01365.x
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956. https://doi.org/10.1111/j.1469-185X.2010.00141.x
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20:831–844. https://doi.org/10.1111/j.1420-9101.2007.01300.x
Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485. https://doi.org/10.1038/nature09210
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pigeon G, Festa-Bianchet M, Pelletier F (2017) Long-term fitness consequences of early environment in a long-lived ungulate. Proc R Soc B 284:20170222. https://doi.org/10.1098/rspb.2017.0222
Plard F, Gaillard JM, Bonenfant C, Mark Hewison AJ, Delorme D, Cargnelutti B, Kjellander P, Nilsen EB, Coulson T (2012) Parturition date for a given female is highly repeatable within five roe deer populations. Biol Lett 9:20120841. https://doi.org/10.1098/rsbl.2012.0841
Plard F, Gaillard JM, Coulson T, Mark Hewison AJ, Delorme D, Warnant C, Bonenfant C (2014) Mismatch between birth date and vegetation phenology slows the demography of roe deer. PLoS Biol 12:e1001828. https://doi.org/10.1371/journal.pbio.1001828
Poirier M-A, Festa-Bianchet M (2018) Social integration and acclimation of translocated bighorn sheep (Ovis canadensis). Biol Conserv 218:1–9. https://doi.org/10.1016/j.biocon.2017.11.031
Porlier M, Charmantier A, Bourgault P, Perret P, Blondel J, Garant D (2012) Variation in phenotypic plasticity and selection patterns in blue tit breeding time: between- and within-population comparisons. J Anim Ecol 81:1041–1051. https://doi.org/10.1111/j.1365-2656.2012.01996.x
Post E, Stenseth NC (1999) Climatic variability, plant phenology, and northern ungulates. Ecology 80:1322–1339
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org
Rioux-Paquette E, Festa-Bianchet M, Coltman DW (2011) Sex-differential effects of inbreeding on overwinter survival, birth date and mass of bighorn lambs. J Evol Biol 24:121–131. https://doi.org/10.1111/j.1420-9101.2010.02154.x
Siepielski AM, Morrissey MB, Buoro M, Carlson SM, Caruso CM, Clegg SM, Coulson T, DiBattista J, Gotanda KM, Francis CD, Hereford J, Kingsolver JG, Augustine KE, Kruuk LEB, Martin RA, Sheldon BC, Sletvold N, Svensson EI, Wade MJ, MacColl ADC (2017) Precipitation drives global variation in natural selection. Science 355:959–962. https://doi.org/10.1126/science.aag2773
Stopher KV, Bento AI, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2014) Multiple pathways mediate effects of climate change on maternal reproductive traits in a red deer population. Ecology 95:3124–3138
Thackeray SJ, Sparks TH, Frederiksen M et al (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Change Biol 16:3304–3313. https://doi.org/10.1111/j.1365-2486.2010.02165.x
Uller T, Nakagawa S, English S (2013) Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol 26:2161–2170. https://doi.org/10.1111/jeb.12212
van de Pol M, Wright J (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav 77:753–758. https://doi.org/10.1016/j.anbehav.2008.11.006
van de Pol M, Bailey LD, McLean N, Rijsdijk L, Lawson CR, Brouwer L (2016) Identifying the best climatic predictors in ecology and evolution. Methods Ecol Evol 7:1246–1257. https://doi.org/10.1111/2041-210X.12590
Veeroja R, Kirk A, Tilgar V, Tõnisson J (2013) Winter climate, age, and population density affect the timing of conception in female moose (Alces alces). Acta Theriol 58:349–357. https://doi.org/10.1007/s13364-012-0106-9
Visser ME, te Marvelde L, Lof ME (2012) Adaptive phenological mismatches of birds and their food in a warming world. J Ornithol 153:75–84. https://doi.org/10.1007/s10336-011-0770-6
Zerbe P, Clauss M, Codron D, Bingaman Lackey L, Rensch E, Streich JW, Hatt JM, Müller DWH (2012) Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation, photoperiodic control, and life history. Biol Rev 87:965–990. https://doi.org/10.1111/j.1469-185X.2012.00238.x
Acknowledgments
We are grateful to all people who helped during fieldwork including S. Guillemette, M.-A. Poirier, S. Tardif and N. Blais. We thank A. Hubbs, C. Feder and J.T. Jorgenson (Alberta Fish & Wildlife) for logistical help. We are especially grateful to A. Bourret and two anonymous reviewers for constructive comments on an earlier draft of the manuscript. L-AR was partly supported by a Doctoral Fellowship from the Université de Sherbrooke, EnviroNord and Hydro-Québec.
Funding
This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery Grants to MFB and FP and doctoral scholarship to GP), the Canada Research Chair program (FP) and the Alberta Conservation Association through research grants to L-AR, FP and MFB.
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Animals were captured and handled in compliance with the Canadian Council on Animal Care, under the approval of the Université de Sherbrooke Animal Care Committee (protocol number FP-2016-01 and MFB-2014-01—Université de Sherbrooke).
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Renaud, LA., Pigeon, G., Festa-Bianchet, M. et al. Phenotypic plasticity in bighorn sheep reproductive phenology: from individual to population. Behav Ecol Sociobiol 73, 50 (2019). https://doi.org/10.1007/s00265-019-2656-1
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DOI: https://doi.org/10.1007/s00265-019-2656-1