Evolution of large males is associated with female-skewed adult sex ratios in amniotes

András Liker; Veronika Bókony; Ivett Pipoly; Jean Francois Lemaître; Jean Michel Gaillard; Tamás Székely; Robert P. Freckleton

doi:10.1111/evo.14273

Evolution of large males is associated with female-skewed adult sex ratios in amniotes

András Liker, Veronika Bókony, Ivett Pipoly, Jean Francois Lemaître, Jean Michel Gaillard, Tamás Székely, Robert P. Freckleton

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Abstract

Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (ASR, the proportion of males in the adult population) should influence SSD because ASR relates to both the number of competitors and available mates, which shape the intensity of mating competition and thereby promotes SSD evolution. However, whether ASR correlates with SSD variation among species has not been yet tested across a broad range of taxa. Using phylogenetic comparative analyses of 462 amniotes (i.e., reptiles, birds, and mammals), we fill this knowledge gap by showing that male bias in SSD increases with increasingly female-skewed ASRs in both mammals and birds. This relationship is not explained by the higher mortality of the larger sex because SSD is not associated with sex differences in either juvenile or adult mortality. Phylogenetic path analysis indicates that higher mortality in one sex leads to skewed ASR, which in turn may generate selection for SSD biased toward the rare sex. Taken together, our findings provide evidence that skewed ASRs in amniote populations can result in the rarer sex evolving large size to capitalize on enhanced mating opportunities.

Original language	English
Pages (from-to)	1636-1649
Number of pages	14
Journal	Evolution
Volume	25
Issue number	7
Early online date	22 May 2021
DOIs	https://doi.org/10.1111/evo.14273
Publication status	Published - 19 Jul 2021

Bibliographical note

Funding Information:
We thank D. Gigler, G. Milne, H. Naylor, and E. Sebestyén for help in data collection; Z. Végvári for calculating environmental variables; and B. Vági for discussions. AL was supported by the National Research, Development and Innovation Office of Hungary (NKFIH, grants KH130430 and K132490), by the Hungarian Academy of Sciences, and by the TKP2020‐IKA‐07 project financed under the 2020–4.1.1‐TKP2020 Thematic Excellence Program by the National Research, Development and Innovation Fund of Hungary. IP was supported by the ÚNKP‐17‐3 New National Excellence Program of the Ministry of Human Capacities. VB was supported by an NKFIH grant (K115402), the János Bolyai Scholarship of the Hungarian Academy of Sciences, and the ÚNKP‐20‐5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund. J‐FL and J‐MG were supported by a grant from the Agence Nationale de la Recherche (ANR‐15‐CE32‐0002‐01). TS and AL were supported by an NKFIH grant (K116310). TS is funded by a Royal Society Wolfson Merit award and by ÉLVONAL KKP‐126949. TS and J‐MG were supported by a grant of the Royal Society‐CNRS (IE160592).

Funding

We thank D. Gigler, G. Milne, H. Naylor, and E. Sebestyén for help in data collection; Z. Végvári for calculating environmental variables; and B. Vági for discussions. AL was supported by the National Research, Development and Innovation Office of Hungary (NKFIH, grants KH130430 and K132490), by the Hungarian Academy of Sciences, and by the TKP2020‐IKA‐07 project financed under the 2020–4.1.1‐TKP2020 Thematic Excellence Program by the National Research, Development and Innovation Fund of Hungary. IP was supported by the ÚNKP‐17‐3 New National Excellence Program of the Ministry of Human Capacities. VB was supported by an NKFIH grant (K115402), the János Bolyai Scholarship of the Hungarian Academy of Sciences, and the ÚNKP‐20‐5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund. J‐FL and J‐MG were supported by a grant from the Agence Nationale de la Recherche (ANR‐15‐CE32‐0002‐01). TS and AL were supported by an NKFIH grant (K116310). TS is funded by a Royal Society Wolfson Merit award and by ÉLVONAL KKP‐126949. TS and J‐MG were supported by a grant of the Royal Society‐CNRS (IE160592). We thank D. Gigler, G. Milne, H. Naylor, and E. Sebesty?n for help in data collection; Z. V?gv?ri for calculating environmental variables; and B. V?gi for discussions. AL was supported by the National Research, Development and Innovation Office of Hungary (NKFIH, grants KH130430 and K132490), by the Hungarian Academy of Sciences, and by the TKP2020-IKA-07 project financed under the 2020?4.1.1-TKP2020 Thematic Excellence Program by the National Research, Development and Innovation Fund of Hungary. IP was supported by the ?NKP-17-3 New National Excellence Program of the Ministry of Human Capacities. VB was supported by an NKFIH grant (K115402), the J?nos Bolyai Scholarship of the Hungarian Academy of Sciences, and the ?NKP-20-5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund. J-FL and J-MG were supported by a grant from the Agence Nationale de la Recherche (ANR-15-CE32-0002-01). TS and AL were supported by an NKFIH grant (K116310). TS is funded by a Royal Society Wolfson Merit award and by ?LVONAL KKP-126949. TS and J-MG were supported by a grant of the Royal Society-CNRS (IE160592).

Keywords

Comparative method
mating competition
mating opportunity
sex-biased mortality
sexual selection

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
General Agricultural and Biological Sciences

Access to Document

10.1111/evo.14273

Evolution_revision_ submitted.PDF
This is the peer reviewed version of the following article: Liker, A., Bókony, V., Pipoly, I., Lemaître, J.-F., Gaillard, J.-M., Székely, T. and Freckleton, R.P. (2021), Evolution of large males is associated with female-skewed adult sex ratios in amniotes. Evolution., which has been published in final form at https://doi.org/10.1111/evo.14273 . This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.
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Cite this

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title = "Evolution of large males is associated with female-skewed adult sex ratios in amniotes",

abstract = "Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (ASR, the proportion of males in the adult population) should influence SSD because ASR relates to both the number of competitors and available mates, which shape the intensity of mating competition and thereby promotes SSD evolution. However, whether ASR correlates with SSD variation among species has not been yet tested across a broad range of taxa. Using phylogenetic comparative analyses of 462 amniotes (i.e., reptiles, birds, and mammals), we fill this knowledge gap by showing that male bias in SSD increases with increasingly female-skewed ASRs in both mammals and birds. This relationship is not explained by the higher mortality of the larger sex because SSD is not associated with sex differences in either juvenile or adult mortality. Phylogenetic path analysis indicates that higher mortality in one sex leads to skewed ASR, which in turn may generate selection for SSD biased toward the rare sex. Taken together, our findings provide evidence that skewed ASRs in amniote populations can result in the rarer sex evolving large size to capitalize on enhanced mating opportunities.",

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author = "Andr{\'a}s Liker and Veronika B{\'o}kony and Ivett Pipoly and Lema{\^i}tre, {Jean Francois} and Gaillard, {Jean Michel} and Tam{\'a}s Sz{\'e}kely and Freckleton, {Robert P.}",

note = "Funding Information: We thank D. Gigler, G. Milne, H. Naylor, and E. Sebesty{\'e}n for help in data collection; Z. V{\'e}gv{\'a}ri for calculating environmental variables; and B. V{\'a}gi for discussions. AL was supported by the National Research, Development and Innovation Office of Hungary (NKFIH, grants KH130430 and K132490), by the Hungarian Academy of Sciences, and by the TKP2020‐IKA‐07 project financed under the 2020–4.1.1‐TKP2020 Thematic Excellence Program by the National Research, Development and Innovation Fund of Hungary. IP was supported by the {\'U}NKP‐17‐3 New National Excellence Program of the Ministry of Human Capacities. VB was supported by an NKFIH grant (K115402), the J{\'a}nos Bolyai Scholarship of the Hungarian Academy of Sciences, and the {\'U}NKP‐20‐5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund. J‐FL and J‐MG were supported by a grant from the Agence Nationale de la Recherche (ANR‐15‐CE32‐0002‐01). TS and AL were supported by an NKFIH grant (K116310). TS is funded by a Royal Society Wolfson Merit award and by {\'E}LVONAL KKP‐126949. TS and J‐MG were supported by a grant of the Royal Society‐CNRS (IE160592). ",

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AU - Liker, András

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AU - Lemaître, Jean Francois

AU - Gaillard, Jean Michel

AU - Székely, Tamás

AU - Freckleton, Robert P.

N1 - Funding Information: We thank D. Gigler, G. Milne, H. Naylor, and E. Sebestyén for help in data collection; Z. Végvári for calculating environmental variables; and B. Vági for discussions. AL was supported by the National Research, Development and Innovation Office of Hungary (NKFIH, grants KH130430 and K132490), by the Hungarian Academy of Sciences, and by the TKP2020‐IKA‐07 project financed under the 2020–4.1.1‐TKP2020 Thematic Excellence Program by the National Research, Development and Innovation Fund of Hungary. IP was supported by the ÚNKP‐17‐3 New National Excellence Program of the Ministry of Human Capacities. VB was supported by an NKFIH grant (K115402), the János Bolyai Scholarship of the Hungarian Academy of Sciences, and the ÚNKP‐20‐5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund. J‐FL and J‐MG were supported by a grant from the Agence Nationale de la Recherche (ANR‐15‐CE32‐0002‐01). TS and AL were supported by an NKFIH grant (K116310). TS is funded by a Royal Society Wolfson Merit award and by ÉLVONAL KKP‐126949. TS and J‐MG were supported by a grant of the Royal Society‐CNRS (IE160592).

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N2 - Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (ASR, the proportion of males in the adult population) should influence SSD because ASR relates to both the number of competitors and available mates, which shape the intensity of mating competition and thereby promotes SSD evolution. However, whether ASR correlates with SSD variation among species has not been yet tested across a broad range of taxa. Using phylogenetic comparative analyses of 462 amniotes (i.e., reptiles, birds, and mammals), we fill this knowledge gap by showing that male bias in SSD increases with increasingly female-skewed ASRs in both mammals and birds. This relationship is not explained by the higher mortality of the larger sex because SSD is not associated with sex differences in either juvenile or adult mortality. Phylogenetic path analysis indicates that higher mortality in one sex leads to skewed ASR, which in turn may generate selection for SSD biased toward the rare sex. Taken together, our findings provide evidence that skewed ASRs in amniote populations can result in the rarer sex evolving large size to capitalize on enhanced mating opportunities.

AB - Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (ASR, the proportion of males in the adult population) should influence SSD because ASR relates to both the number of competitors and available mates, which shape the intensity of mating competition and thereby promotes SSD evolution. However, whether ASR correlates with SSD variation among species has not been yet tested across a broad range of taxa. Using phylogenetic comparative analyses of 462 amniotes (i.e., reptiles, birds, and mammals), we fill this knowledge gap by showing that male bias in SSD increases with increasingly female-skewed ASRs in both mammals and birds. This relationship is not explained by the higher mortality of the larger sex because SSD is not associated with sex differences in either juvenile or adult mortality. Phylogenetic path analysis indicates that higher mortality in one sex leads to skewed ASR, which in turn may generate selection for SSD biased toward the rare sex. Taken together, our findings provide evidence that skewed ASRs in amniote populations can result in the rarer sex evolving large size to capitalize on enhanced mating opportunities.

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Evolution of large males is associated with female-skewed adult sex ratios in amniotes

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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