Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction

Emeline Mourocq; Pierre Bize; Sandra Bouwhuis; Russell Bradley; Anne Charmantier; Carlos de la Cruz; Szymon M Drobniak; Richard H M Espie; Márton Herényi; Hermann Hötker; Oliver Krüger; John Marzluff; Anders P Møller; Shinichi Nakagawa; Richard A Phillips; Andrew N Radford; Alexandre Roulin; János Török; Juliana Valencia; Martijn van de Pol; Ian G Warkentin; Isabel S Winney; Andrew G Wood; Michael Griesser

doi:10.1111/evo.12853

Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction

Emeline Mourocq, Pierre Bize, Sandra Bouwhuis, Russell Bradley, Anne Charmantier, Carlos de la Cruz, Szymon M Drobniak, Richard H M Espie, Márton Herényi, Hermann Hötker, Oliver Krüger, John Marzluff, Anders P Møller, Shinichi Nakagawa, Richard A Phillips, Andrew N Radford, Alexandre Roulin, János Török, Juliana Valencia, Martijn van de PolIan G Warkentin, Isabel S Winney, Andrew G Wood, Michael Griesser

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

28 Citations (Scopus)

Abstract

Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR-fitness relationship only has been investigated intraspecifically. Here we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species-specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life-history as well as social and ecological factors. Most individuals adopted the species-specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with lifespan. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long lifespan and costs of early reproduction. By providing the first empirical confirmations of key predictions of life-history theory across species, this study contributes to a better understanding of life-history evolution. This article is protected by copyright. All rights reserved.

Original language	English
Pages (from-to)	296-313
Number of pages	18
Journal	Evolution
Volume	70
Issue number	2
Early online date	5 Feb 2016
DOIs	https://doi.org/10.1111/evo.12853
Publication status	Published - Feb 2016

Bibliographical note

ACKNOWLEDGMENTS
The authors thank B. Hatchwell for contributing the long-tailed tit data, B. Kempenaers and E. Schlicht for contributing blue tit data; B. Sheldon for contributing the blue tit, great tit, and mute swan data; C. Perrins for contributing the mute swan data and T. Burkefor contributing the house sparrow data. They thank E. Postma and J. D. Ibáñez Álamo for relevant discussions. They also thank to the numerous fieldworkers and funding agencies that contributed to these long-term studies. This study was financed by the Swiss National Research Foundation (grant numbers PPOOP3_123520 and PPOOP3_150752 to MG). PB, SB, RB, AC, CC, RE, MH, HH, OK, JM, AM, SN, RP, ANR, AR, JT, JV, MVP, IGW, ISW, AW provided unpublished data on lifetime reproductive success. EM compiled the data, performed the statistical analysis, and wrote the first draft of the manuscript. All authors contributed to revisions (especially MG) and gave final approval for publication. MG helped with data compilation and reflection on the manuscript. SMD, SN, and MG helped with the statistical methods and estimation of the indices. SMD wrote the R script to automate the estimation of two indices. The authors have no conflict of interest.

DATA ARCHIVING
The doi for our data is http://dx.doi.org/10.5061/dryad.dk8q3.

This article is protected by copyright. All rights reserved.

Keywords

age at first reproduction
comparative method
cost of reproduction
family formation theory
life-history theory

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Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction
Mourocq, E. (Creator), Bize, P. (Creator), Bouwhuis, S. (Creator), Bradley, R. (Creator), Charmantier, A. (Creator), Cruz, C. D. L. (Creator), Drobniak, S. M. (Creator), Espie, R. H. M. (Creator), Herényi, M. (Creator), Hötker, H. (Creator), Krüger, O. (Creator), Marzluff, J. (Creator), Møller, A. P. (Creator), Nakagawa, S. (Creator), Phillips, R. A. (Creator), Radford, A. N. (Creator), Roulin, A. (Creator), Török, J. (Creator), Valencia, J. (Creator), Pol, M. V. D. (Creator), Warkentin, I. G. (Creator), Winney, I. S. (Creator), Wood, A. G. (Creator), Griesser, M. (Creator) & Paton, G. (Data Manager), Dryad Digital Repository, 7 Jan 2016
DOI: 10.5061/dryad.dk8q3
Dataset

Cite this

Mourocq, E., Bize, P., Bouwhuis, S., Bradley, R., Charmantier, A., Cruz, C. D. L., Drobniak, S. M., Espie, R. H. M., Herényi, M., Hötker, H., Krüger, O., Marzluff, J., Møller, A. P., Nakagawa, S., Phillips, R. A., Radford, A. N., Roulin, A., Török, J., Valencia, J., ... Griesser, M. (2016). Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction. Evolution, 70(2), 296-313. https://doi.org/10.1111/evo.12853

Mourocq, E, Bize, P, Bouwhuis, S, Bradley, R, Charmantier, A, Cruz, CDL, Drobniak, SM, Espie, RHM, Herényi, M, Hötker, H, Krüger, O, Marzluff, J, Møller, AP, Nakagawa, S, Phillips, RA, Radford, AN, Roulin, A, Török, J, Valencia, J, Pol, MVD, Warkentin, IG, Winney, IS, Wood, AG & Griesser, M 2016, 'Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction', Evolution, vol. 70, no. 2, pp. 296-313. https://doi.org/10.1111/evo.12853

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title = "Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction",

abstract = "Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR-fitness relationship only has been investigated intraspecifically. Here we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species-specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life-history as well as social and ecological factors. Most individuals adopted the species-specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with lifespan. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long lifespan and costs of early reproduction. By providing the first empirical confirmations of key predictions of life-history theory across species, this study contributes to a better understanding of life-history evolution. This article is protected by copyright. All rights reserved.",

keywords = "age at first reproduction, comparative method, cost of reproduction, family formation theory, life-history theory",

author = "Emeline Mourocq and Pierre Bize and Sandra Bouwhuis and Russell Bradley and Anne Charmantier and Cruz, {Carlos de la} and Drobniak, {Szymon M} and Espie, {Richard H M} and M{\'a}rton Her{\'e}nyi and Hermann H{\"o}tker and Oliver Kr{\"u}ger and John Marzluff and M{\o}ller, {Anders P} and Shinichi Nakagawa and Phillips, {Richard A} and Radford, {Andrew N} and Alexandre Roulin and J{\'a}nos T{\"o}r{\"o}k and Juliana Valencia and Pol, {Martijn van de} and Warkentin, {Ian G} and Winney, {Isabel S} and Wood, {Andrew G} and Michael Griesser",

note = "ACKNOWLEDGMENTS The authors thank B. Hatchwell for contributing the long-tailed tit data, B. Kempenaers and E. Schlicht for contributing blue tit data; B. Sheldon for contributing the blue tit, great tit, and mute swan data; C. Perrins for contributing the mute swan data and T. Burkefor contributing the house sparrow data. They thank E. Postma and J. D. Ib{\'a}{\~n}ez {\'A}lamo for relevant discussions. They also thank to the numerous fieldworkers and funding agencies that contributed to these long-term studies. This study was financed by the Swiss National Research Foundation (grant numbers PPOOP3_123520 and PPOOP3_150752 to MG). PB, SB, RB, AC, CC, RE, MH, HH, OK, JM, AM, SN, RP, ANR, AR, JT, JV, MVP, IGW, ISW, AW provided unpublished data on lifetime reproductive success. EM compiled the data, performed the statistical analysis, and wrote the first draft of the manuscript. All authors contributed to revisions (especially MG) and gave final approval for publication. MG helped with data compilation and reflection on the manuscript. SMD, SN, and MG helped with the statistical methods and estimation of the indices. SMD wrote the R script to automate the estimation of two indices. The authors have no conflict of interest. DATA ARCHIVING The doi for our data is http://dx.doi.org/10.5061/dryad.dk8q3. This article is protected by copyright. All rights reserved.",

year = "2016",

month = feb,

doi = "10.1111/evo.12853",

language = "English",

volume = "70",

pages = "296--313",

journal = "Evolution",

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T1 - Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction

AU - Mourocq, Emeline

AU - Bize, Pierre

AU - Bouwhuis, Sandra

AU - Bradley, Russell

AU - Charmantier, Anne

AU - Cruz, Carlos de la

AU - Drobniak, Szymon M

AU - Espie, Richard H M

AU - Herényi, Márton

AU - Hötker, Hermann

AU - Krüger, Oliver

AU - Marzluff, John

AU - Møller, Anders P

AU - Nakagawa, Shinichi

AU - Phillips, Richard A

AU - Radford, Andrew N

AU - Roulin, Alexandre

AU - Török, János

AU - Valencia, Juliana

AU - Pol, Martijn van de

AU - Warkentin, Ian G

AU - Winney, Isabel S

AU - Wood, Andrew G

AU - Griesser, Michael

N1 - ACKNOWLEDGMENTS The authors thank B. Hatchwell for contributing the long-tailed tit data, B. Kempenaers and E. Schlicht for contributing blue tit data; B. Sheldon for contributing the blue tit, great tit, and mute swan data; C. Perrins for contributing the mute swan data and T. Burkefor contributing the house sparrow data. They thank E. Postma and J. D. Ibáñez Álamo for relevant discussions. They also thank to the numerous fieldworkers and funding agencies that contributed to these long-term studies. This study was financed by the Swiss National Research Foundation (grant numbers PPOOP3_123520 and PPOOP3_150752 to MG). PB, SB, RB, AC, CC, RE, MH, HH, OK, JM, AM, SN, RP, ANR, AR, JT, JV, MVP, IGW, ISW, AW provided unpublished data on lifetime reproductive success. EM compiled the data, performed the statistical analysis, and wrote the first draft of the manuscript. All authors contributed to revisions (especially MG) and gave final approval for publication. MG helped with data compilation and reflection on the manuscript. SMD, SN, and MG helped with the statistical methods and estimation of the indices. SMD wrote the R script to automate the estimation of two indices. The authors have no conflict of interest. DATA ARCHIVING The doi for our data is http://dx.doi.org/10.5061/dryad.dk8q3. This article is protected by copyright. All rights reserved.

PY - 2016/2

Y1 - 2016/2

N2 - Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR-fitness relationship only has been investigated intraspecifically. Here we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species-specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life-history as well as social and ecological factors. Most individuals adopted the species-specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with lifespan. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long lifespan and costs of early reproduction. By providing the first empirical confirmations of key predictions of life-history theory across species, this study contributes to a better understanding of life-history evolution. This article is protected by copyright. All rights reserved.

AB - Fitness can be profoundly influenced by the age at first reproduction (AFR), but to date the AFR-fitness relationship only has been investigated intraspecifically. Here we investigated the relationship between AFR and average lifetime reproductive success (LRS) across 34 bird species. We assessed differences in the deviation of the Optimal AFR (i.e., the species-specific AFR associated with the highest LRS) from the age at sexual maturity, considering potential effects of life-history as well as social and ecological factors. Most individuals adopted the species-specific Optimal AFR and both the mean and Optimal AFR of species correlated positively with lifespan. Interspecific deviations of the Optimal AFR were associated with indices reflecting a change in LRS or survival as a function of AFR: a delayed AFR was beneficial in species where early AFR was associated with a decrease in subsequent survival or reproductive output. Overall, our results suggest that a delayed onset of reproduction beyond maturity is an optimal strategy explained by a long lifespan and costs of early reproduction. By providing the first empirical confirmations of key predictions of life-history theory across species, this study contributes to a better understanding of life-history evolution. This article is protected by copyright. All rights reserved.

KW - age at first reproduction

KW - comparative method

KW - cost of reproduction

KW - family formation theory

KW - life-history theory

U2 - 10.1111/evo.12853

DO - 10.1111/evo.12853

M3 - Article

C2 - 26763090

SN - 0014-3820

VL - 70

SP - 296

EP - 313

JO - Evolution

JF - Evolution

IS - 2

ER -

Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction

Abstract

Bibliographical note

Keywords

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Lifespan and reproductive cost explain interspecific variation in the optimal onset of reproduction

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