Fluctuating optimum and temporally variable selection on breeding date in birds and mammals

Pierre de Villemereuil* (Corresponding Author), Anne Charmantier, Debora Arlt, Pierre Bize, Patricia Brekke, Lyanne Brouwer, Andrew Cockburn, Steeve D Côté, F. Stephen Dobson, Simon R. Evans, Marco Festa-Bianchet, Marlène Gamelon, Sandra Hamel, Johann Hegelbach, Kurt Jerstad, Bart Kempenaers, Loeske E.B. Kruuk, Jouko Kumpula, Thomas Kvalnes, Andrew G. McAdamS. Eryn McFarlane, Michael B. Morrissey, Tomas Pärt, Josephine M. Pemberton, Anna Qvarnström, Ole-Wiggo Røstad, Julia Schroeder, Juan Carlos Senar, Ben C. Sheldon, Martijn van de Pol, Marcel E Visser, Nathaniel T Wheelwright, Jarle Tufto, Luis-Miguel Chevin* (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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Abstract

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.
Original languageEnglish
Pages (from-to)31969-31978
Number of pages10
JournalPNAS
Volume117
Issue number50
Early online date30 Nov 2020
DOIs
Publication statusPublished - 15 Dec 2020

Bibliographical note

Acknowledgments:
We thank Timothée Bonnet for useful discussions. L-M.C. and P.d.V. acknowledge support from the European Research Council (ERC) (Grant 678140-FluctEvol). The Montpellier tit group acknowledges the long-term support of the Observatoire des Sciences de l’Univers – Observatoire de REcherche Montpelliérain de l’Environnement (OSU-OREME). The bighorn, mountain goat, and eastern gray kangaroo studies were supported by Natural Sciences and Engineering Research Council (NSERC) of Canada. Recent data collection for Wytham has been provided by grants from Biotechnology and Biological Sciences Research Council (BB/L006081/1), ERC (AdG250164), and the UK Natural Environment Research Council (NERC) (NE/K006274/1, NE/S010335/1). The Columbian ground squirrel study was supported by the National Science Foundation (Grant DEB-0089473). Trait and fitness data for hihi were collected/managed by John Ewen under New Zealand Department of Conservation hihi management contracts and research permits AK/15073/RES, AK-24128-FAU, 36186-FAU, and 44300-FAU and with additional financial support via NERC UK, The Leverhulme Trust UK, Marsden Fund New Zealand, and the Hihi Conservation Charitable Trust. The data on reindeer were made available through the Reindeer husbandry in a Globalizing North Nordic Center of Excellence, and the crew at Kutuharju Experimental Reindeer Research Station in the Reindeer Herder’s Association are thanked for their valuable assistance and logistic support in data collection. The red deer, Silwood blue tit, and Soay sheep datasets were supported by UK NERC. Lundy sparrow data were supported by NERC, a Marie Skłodowska-Curie Action, and Volkswagenstiftung. The red squirrel project was funded by NSERC of Canada and the National Science Foundation. J.C.S. was supported by a grant from the Ministry of Economy and Competitivity, Spanish Research Council (CGL-2016-79568-C3-3-P). J.T., T.K., and M.G. were supported by the Research Council of Norway through its Centers for Excellence funding scheme, Project 223257. Research on fairy wrens has been supported by the Australian Research Council. The Northern wheatear and the flycatcher studies were supported by grants from the Swedish Research Council VR. We thank the many agencies that funded long-term studies and the hundreds of people that participated in fieldwork.

Keywords

  • adaptation
  • fluctuating enviroment
  • fitness landscape
  • meta-analysis
  • Phenotic plasticity

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