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

Pierre de Villemereuil; 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 McAdam; S. 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; M.E. Visser; Nathaniel T. Wheelwright; Jarle Tufto; Luis-Miguel Chevin

doi:10.1073/pnas.2009003117

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

Pierre de Villemereuil, 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 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, M.E. Visser, Nathaniel T. Wheelwright, Jarle Tufto, Luis-Miguel Chevin

NIOO - Animal Ecology (AnE)

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

Samenvatting

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.

Originele taal-2	Engels
Pagina's (van-tot)	31969-31978
Tijdschrift	Proceedings of the National Academy of Sciences of the United States of America
Volume	117
Nummer van het tijdschrift	50
DOI's	https://doi.org/10.1073/pnas.2009003117
Status	Gepubliceerd - 2020

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10.1073/pnas.2009003117

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de Villemereuil, P., Charmantier, A., Arlt, D., Bize, P., Brekke, P., Brouwer, L., Cockburn, A., Côté, S. D., Dobson, F. S., Evans, S. R., Festa-Bianchet, M., Gamelon, M., Hamel, S., Hegelbach, J., Jerstad, K., Kempenaers, B., Kruuk, L. E. B., Kumpula, J., Kvalnes, T., ... Chevin, L-M. (2020). Fluctuating optimum and temporally variable selection on breeding date in birds and mammals. Proceedings of the National Academy of Sciences of the United States of America, 117(50), 31969-31978. https://doi.org/10.1073/pnas.2009003117

de Villemereuil, Pierre ; Charmantier, Anne ; Arlt, Debora ; Bize, Pierre ; Brekke, Patricia ; Brouwer, Lyanne ; Cockburn, Andrew ; Côté, Steeve D ; Dobson, F. Stephen ; Evans, Simon R. ; Festa-Bianchet, Marco ; Gamelon, Marlène ; Hamel, Sandra ; Hegelbach, Johann ; Jerstad, Kurt ; Kempenaers, Bart ; Kruuk, Loeske E.B. ; Kumpula, Jouko ; Kvalnes, Thomas ; McAdam, Andrew ; McFarlane, S. Eryn ; Morrissey, Michael B. ; Pärt, Tomas ; Pemberton, Josephine M. ; Qvarnström, Anna ; Røstad, Ole Wiggo ; Schroeder, Julia ; Senar, Juan Carlos ; Sheldon, Ben C. ; van de Pol, Martijn ; Visser, M.E. ; Wheelwright, Nathaniel T. ; Tufto, Jarle ; Chevin, Luis-Miguel. / Fluctuating optimum and temporally variable selection on breeding date in birds and mammals. In: Proceedings of the National Academy of Sciences of the United States of America. 2020 ; Vol. 117, Nr. 50. blz. 31969-31978.

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title = "Fluctuating optimum and temporally variable selection on breeding date in birds and mammals",

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.",

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author = "{de Villemereuil}, Pierre and Anne Charmantier and Debora Arlt and Pierre Bize and Patricia Brekke and Lyanne Brouwer and Andrew Cockburn and C{\^o}t{\'e}, {Steeve D} and Dobson, {F. Stephen} and Evans, {Simon R.} and Marco Festa-Bianchet and Marl{\`e}ne Gamelon and Sandra Hamel and Johann Hegelbach and Kurt Jerstad and Bart Kempenaers and Kruuk, {Loeske E.B.} and Jouko Kumpula and Thomas Kvalnes and Andrew McAdam and McFarlane, {S. Eryn} and Morrissey, {Michael B.} and Tomas P{\"a}rt and Pemberton, {Josephine M.} and Anna Qvarnstr{\"o}m and R{\o}stad, {Ole Wiggo} and Julia Schroeder and Senar, {Juan Carlos} and Sheldon, {Ben C.} and {van de Pol}, Martijn and M.E. Visser and Wheelwright, {Nathaniel T.} and Jarle Tufto and Luis-Miguel Chevin",

note = "7120,AnE; Data archiving: no NIOO data",

year = "2020",

doi = "10.1073/pnas.2009003117",

language = "English",

volume = "117",

pages = "31969--31978",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

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publisher = "National Academy of Sciences",

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de Villemereuil, P, Charmantier, A, Arlt, D, Bize, P, Brekke, P, Brouwer, L, Cockburn, A, Côté, SD, Dobson, FS, Evans, SR, Festa-Bianchet, M, Gamelon, M, Hamel, S, Hegelbach, J, Jerstad, K, Kempenaers, B, Kruuk, LEB, Kumpula, J, Kvalnes, T, McAdam, A, McFarlane, SE, Morrissey, MB, Pärt, T, Pemberton, JM, Qvarnström, A, Røstad, OW, Schroeder, J, Senar, JC, Sheldon, BC, van de Pol, M , Visser, ME, Wheelwright, NT, Tufto, J & Chevin, L-M 2020, 'Fluctuating optimum and temporally variable selection on breeding date in birds and mammals', Proceedings of the National Academy of Sciences of the United States of America, vol. 117, nr. 50, blz. 31969-31978. https://doi.org/10.1073/pnas.2009003117

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals. / de Villemereuil, Pierre; Charmantier, Anne; Arlt, Debora; Bize, Pierre; Brekke, Patricia; Brouwer, Lyanne; Cockburn, Andrew; Côté, Steeve D; Dobson, F. Stephen; Evans, Simon R.; Festa-Bianchet, Marco; Gamelon, Marlène; Hamel, Sandra; Hegelbach, Johann; Jerstad, Kurt; Kempenaers, Bart; Kruuk, Loeske E.B.; Kumpula, Jouko; Kvalnes, Thomas; McAdam, Andrew; McFarlane, S. Eryn; Morrissey, Michael B.; Pärt, Tomas; Pemberton, Josephine M.; Qvarnström, Anna; Røstad, Ole Wiggo; Schroeder, Julia; Senar, Juan Carlos; Sheldon, Ben C.; van de Pol, Martijn ; Visser, M.E.; Wheelwright, Nathaniel T.; Tufto, Jarle; Chevin, Luis-Miguel.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 117, Nr. 50, 2020, blz. 31969-31978.

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

TY - JOUR

T1 - Fluctuating optimum and temporally variable selection on breeding date in birds and mammals

AU - de Villemereuil, Pierre

AU - Charmantier, Anne

AU - Arlt, Debora

AU - Bize, Pierre

AU - Brekke, Patricia

AU - Brouwer, Lyanne

AU - Cockburn, Andrew

AU - Côté, Steeve D

AU - Dobson, F. Stephen

AU - Evans, Simon R.

AU - Festa-Bianchet, Marco

AU - Gamelon, Marlène

AU - Hamel, Sandra

AU - Hegelbach, Johann

AU - Jerstad, Kurt

AU - Kempenaers, Bart

AU - Kruuk, Loeske E.B.

AU - Kumpula, Jouko

AU - Kvalnes, Thomas

AU - McAdam, Andrew

AU - McFarlane, S. Eryn

AU - Morrissey, Michael B.

AU - Pärt, Tomas

AU - Pemberton, Josephine M.

AU - Qvarnström, Anna

AU - Røstad, Ole Wiggo

AU - Schroeder, Julia

AU - Senar, Juan Carlos

AU - Sheldon, Ben C.

AU - van de Pol, Martijn

AU - Visser, M.E.

AU - Wheelwright, Nathaniel T.

AU - Tufto, Jarle

AU - Chevin, Luis-Miguel

N1 - 7120,AnE; Data archiving: no NIOO data

PY - 2020

Y1 - 2020

N2 - 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.

AB - 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.

KW - international

KW - Plan_S-Compliant_NO

U2 - 10.1073/pnas.2009003117

DO - 10.1073/pnas.2009003117

M3 - Article

VL - 117

SP - 31969

EP - 31978

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 50

ER -