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Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from tha...

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Autores principales: Chung, Meng‐Han Joseph, Jennions, Michael D., Fox, Rebecca J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8327938/
https://www.ncbi.nlm.nih.gov/pubmed/34367658
http://dx.doi.org/10.1002/evl3.228
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author Chung, Meng‐Han Joseph
Jennions, Michael D.
Fox, Rebecca J.
author_facet Chung, Meng‐Han Joseph
Jennions, Michael D.
Fox, Rebecca J.
author_sort Chung, Meng‐Han Joseph
collection PubMed
description Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.
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spelling pubmed-83279382021-08-06 Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort Chung, Meng‐Han Joseph Jennions, Michael D. Fox, Rebecca J. Evol Lett Letters Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate. John Wiley and Sons Inc. 2021-05-27 /pmc/articles/PMC8327938/ /pubmed/34367658 http://dx.doi.org/10.1002/evl3.228 Text en © 2021 The Authors. Evolution Letters published by Wiley Periodicals LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Letters
Chung, Meng‐Han Joseph
Jennions, Michael D.
Fox, Rebecca J.
Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title_full Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title_fullStr Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title_full_unstemmed Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title_short Quantifying the costs of pre‐ and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort
title_sort quantifying the costs of pre‐ and postcopulatory traits for males: evidence that costs of ejaculation are minor relative to mating effort
topic Letters
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8327938/
https://www.ncbi.nlm.nih.gov/pubmed/34367658
http://dx.doi.org/10.1002/evl3.228
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