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The effects of male age, sperm age and mating history on ejaculate senescence
In polyandrous species, a male’s reproductive success depends on his ability to fertilize females, which, in turn, depends on his mating ability and his ability to produce competitive ejaculates. In many species, sperm traits differ between old and young males in ways that are likely to decrease the...
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Published in: | Functional ecology 2019-07, Vol.33 (7), p.1267-1279 |
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description | In polyandrous species, a male’s reproductive success depends on his ability to fertilize females, which, in turn, depends on his mating ability and his ability to produce competitive ejaculates. In many species, sperm traits differ between old and young males in ways that are likely to decrease the sperm competitiveness and fertility of older males. This age–ejaculate quality relationship is attributed to male ageing (i.e., senescence).
In a natural setting, male age and mating history are usually confounded: older males have usually mated and replenished their sperm supplies more often, so they have made a greater lifetime reproductive effort. In principle, the costs of reproduction, independent of any causal effect of male age, could generate an age‐related decline in ejaculate quality.
To date, only a handful of studies have determined how male age, reproductive effort or their interaction affect ejaculate quality. Here, we experimentally manipulated the long‐term mating history of 209 adult male mosquitofish (Gambusia holbrooki) over 14 weeks (N = 1,118 sperm samples). Males either had direct access to females and could mate freely, or had only visual and olfactory access to females. We documented the effect of mating history, adult male age (3, 9 and 14 weeks post‐maturation) and their interaction on sperm velocity, sperm reserves and the rate of sperm replenishment. For sperm velocity, we additionally examined the effects of sperm age, because when older males mate less (or more) often than younger males there will be a correlation between mean sperm age and male age.
Sexually active males produced fewer sperm and replenished their sperm at a lower rate, and their sperm had lower velocity than males prevented from mating. Though older males produced more sperm, the rate of replenishment and velocity of their sperm was lower than the sperm of younger males. We also tested for a difference in the velocity of recently replenished ( |
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In a natural setting, male age and mating history are usually confounded: older males have usually mated and replenished their sperm supplies more often, so they have made a greater lifetime reproductive effort. In principle, the costs of reproduction, independent of any causal effect of male age, could generate an age‐related decline in ejaculate quality.
To date, only a handful of studies have determined how male age, reproductive effort or their interaction affect ejaculate quality. Here, we experimentally manipulated the long‐term mating history of 209 adult male mosquitofish (Gambusia holbrooki) over 14 weeks (N = 1,118 sperm samples). Males either had direct access to females and could mate freely, or had only visual and olfactory access to females. We documented the effect of mating history, adult male age (3, 9 and 14 weeks post‐maturation) and their interaction on sperm velocity, sperm reserves and the rate of sperm replenishment. For sperm velocity, we additionally examined the effects of sperm age, because when older males mate less (or more) often than younger males there will be a correlation between mean sperm age and male age.
Sexually active males produced fewer sperm and replenished their sperm at a lower rate, and their sperm had lower velocity than males prevented from mating. Though older males produced more sperm, the rate of replenishment and velocity of their sperm was lower than the sperm of younger males. We also tested for a difference in the velocity of recently replenished (<24 hr) and older sperm (i.e., post‐meiotic sperm senescence). There was no evidence that male age or mating history affects the extent of sperm senescence, but older sperm swam faster than recently produced sperm. Crucially, complex interactions are evident between male age and male mating history with respect to sperm number and the proportion of sperm that are replenished.
These results suggest that male age and mating history will interact to determine the reproductive success of a male under sperm competition. They reveal a complex relationship between a male’s age and his ejaculate quality. We suggest that both mating history and sperm age should be controlled for when measuring the intrinsic rate of senescence for male reproductive traits if the goal is to isolate effects that are solely attributable to a male’s chronological age.
A plain language summary is available for this article.
Plain Language Summary</description><identifier>ISSN: 0269-8463</identifier><identifier>ISSN: 1365-2435</identifier><identifier>EISSN: 1365-2435</identifier><identifier>DOI: 10.1111/1365-2435.13305</identifier><language>eng</language><publisher>London: Wiley Subscription Services, Inc</publisher><subject>Age ; ageing ; Aging ; Aging (natural) ; Animal reproduction ; Breeding success ; Chronology ; Competitiveness ; Death benefits ; Females ; Fertility ; Males ; Mating ; mating experience ; Meiosis ; mosquitofish ; Replenishment ; Reproduction ; Reproductive effort ; Senescence ; sexual selection ; Sperm ; Sperm competition ; sperm quality ; Universal life ; Velocity</subject><ispartof>Functional ecology, 2019-07, Vol.33 (7), p.1267-1279</ispartof><rights>2019 The Authors. Functional Ecology © 2019 British Ecological Society</rights><rights>Functional Ecology © 2019 British Ecological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3935-e027f41cea5f7ac732fe06f84e1bc2b6d5d082f8ea740990f3462eaca8d3b2aa3</citedby><cites>FETCH-LOGICAL-c3935-e027f41cea5f7ac732fe06f84e1bc2b6d5d082f8ea740990f3462eaca8d3b2aa3</cites><orcidid>0000-0003-4349-8163 ; 0000-0002-8123-7661 ; 0000-0001-9221-2788 ; 0000-0003-3442-4189 ; 0000-0003-0349-7967</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-179724$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Priest, Nick</contributor><creatorcontrib>Vega‐Trejo, Regina</creatorcontrib><creatorcontrib>Fox, Rebecca J.</creatorcontrib><creatorcontrib>Iglesias‐Carrasco, Maider</creatorcontrib><creatorcontrib>Head, Megan L.</creatorcontrib><creatorcontrib>Jennions, Michael D.</creatorcontrib><creatorcontrib>Priest, Nick</creatorcontrib><title>The effects of male age, sperm age and mating history on ejaculate senescence</title><title>Functional ecology</title><description>In polyandrous species, a male’s reproductive success depends on his ability to fertilize females, which, in turn, depends on his mating ability and his ability to produce competitive ejaculates. In many species, sperm traits differ between old and young males in ways that are likely to decrease the sperm competitiveness and fertility of older males. This age–ejaculate quality relationship is attributed to male ageing (i.e., senescence).
In a natural setting, male age and mating history are usually confounded: older males have usually mated and replenished their sperm supplies more often, so they have made a greater lifetime reproductive effort. In principle, the costs of reproduction, independent of any causal effect of male age, could generate an age‐related decline in ejaculate quality.
To date, only a handful of studies have determined how male age, reproductive effort or their interaction affect ejaculate quality. Here, we experimentally manipulated the long‐term mating history of 209 adult male mosquitofish (Gambusia holbrooki) over 14 weeks (N = 1,118 sperm samples). Males either had direct access to females and could mate freely, or had only visual and olfactory access to females. We documented the effect of mating history, adult male age (3, 9 and 14 weeks post‐maturation) and their interaction on sperm velocity, sperm reserves and the rate of sperm replenishment. For sperm velocity, we additionally examined the effects of sperm age, because when older males mate less (or more) often than younger males there will be a correlation between mean sperm age and male age.
Sexually active males produced fewer sperm and replenished their sperm at a lower rate, and their sperm had lower velocity than males prevented from mating. Though older males produced more sperm, the rate of replenishment and velocity of their sperm was lower than the sperm of younger males. We also tested for a difference in the velocity of recently replenished (<24 hr) and older sperm (i.e., post‐meiotic sperm senescence). There was no evidence that male age or mating history affects the extent of sperm senescence, but older sperm swam faster than recently produced sperm. Crucially, complex interactions are evident between male age and male mating history with respect to sperm number and the proportion of sperm that are replenished.
These results suggest that male age and mating history will interact to determine the reproductive success of a male under sperm competition. They reveal a complex relationship between a male’s age and his ejaculate quality. We suggest that both mating history and sperm age should be controlled for when measuring the intrinsic rate of senescence for male reproductive traits if the goal is to isolate effects that are solely attributable to a male’s chronological age.
A plain language summary is available for this article.
Plain Language Summary</description><subject>Age</subject><subject>ageing</subject><subject>Aging</subject><subject>Aging (natural)</subject><subject>Animal reproduction</subject><subject>Breeding success</subject><subject>Chronology</subject><subject>Competitiveness</subject><subject>Death benefits</subject><subject>Females</subject><subject>Fertility</subject><subject>Males</subject><subject>Mating</subject><subject>mating experience</subject><subject>Meiosis</subject><subject>mosquitofish</subject><subject>Replenishment</subject><subject>Reproduction</subject><subject>Reproductive effort</subject><subject>Senescence</subject><subject>sexual selection</subject><subject>Sperm</subject><subject>Sperm competition</subject><subject>sperm quality</subject><subject>Universal life</subject><subject>Velocity</subject><issn>0269-8463</issn><issn>1365-2435</issn><issn>1365-2435</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNqFkEtPwzAQhC0EEqVw5mqJa9P6EedxrEoLSEVcClfLcdZtqjQOdqIq_56EoF7Zy65GM6PVh9AjJXPaz4LySAQs5GJOOSfiCk0uyjWaEBalQRJG_BbdeX8khKSCsQl63x0AgzGgG4-twSdVAlZ7mGFfgzsNJ1ZV3utNUe3xofCNdR22FYaj0m2pGsAeKvAaKg336Mao0sPD356iz816t3oNth8vb6vlNtA85SIAwmITUg1KmFjpmDMDJDJJCDTTLItykZOEmQRUHJI0JYaHEQOlVZLzjCnFp2g29voz1G0ma1eclOukVYV8Lr6W0rq99K2kcRr3AKboabTXzn634Bt5tK2r-g8lY4ImUcySwbUYXdpZ7x2YSy0lckAsB6ByACp_EfcJMSbORQndf3a5Wa_G3A_Bb3z2</recordid><startdate>201907</startdate><enddate>201907</enddate><creator>Vega‐Trejo, Regina</creator><creator>Fox, Rebecca J.</creator><creator>Iglesias‐Carrasco, Maider</creator><creator>Head, Megan L.</creator><creator>Jennions, Michael D.</creator><creator>Priest, Nick</creator><general>Wiley Subscription Services, Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>DG7</scope><orcidid>https://orcid.org/0000-0003-4349-8163</orcidid><orcidid>https://orcid.org/0000-0002-8123-7661</orcidid><orcidid>https://orcid.org/0000-0001-9221-2788</orcidid><orcidid>https://orcid.org/0000-0003-3442-4189</orcidid><orcidid>https://orcid.org/0000-0003-0349-7967</orcidid></search><sort><creationdate>201907</creationdate><title>The effects of male age, sperm age and mating history on ejaculate senescence</title><author>Vega‐Trejo, Regina ; Fox, Rebecca J. ; Iglesias‐Carrasco, Maider ; Head, Megan L. ; Jennions, Michael D. ; Priest, Nick</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3935-e027f41cea5f7ac732fe06f84e1bc2b6d5d082f8ea740990f3462eaca8d3b2aa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Age</topic><topic>ageing</topic><topic>Aging</topic><topic>Aging (natural)</topic><topic>Animal reproduction</topic><topic>Breeding success</topic><topic>Chronology</topic><topic>Competitiveness</topic><topic>Death benefits</topic><topic>Females</topic><topic>Fertility</topic><topic>Males</topic><topic>Mating</topic><topic>mating experience</topic><topic>Meiosis</topic><topic>mosquitofish</topic><topic>Replenishment</topic><topic>Reproduction</topic><topic>Reproductive effort</topic><topic>Senescence</topic><topic>sexual selection</topic><topic>Sperm</topic><topic>Sperm competition</topic><topic>sperm quality</topic><topic>Universal life</topic><topic>Velocity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vega‐Trejo, Regina</creatorcontrib><creatorcontrib>Fox, Rebecca J.</creatorcontrib><creatorcontrib>Iglesias‐Carrasco, Maider</creatorcontrib><creatorcontrib>Head, Megan L.</creatorcontrib><creatorcontrib>Jennions, Michael D.</creatorcontrib><creatorcontrib>Priest, Nick</creatorcontrib><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Stockholms universitet</collection><jtitle>Functional ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vega‐Trejo, Regina</au><au>Fox, Rebecca J.</au><au>Iglesias‐Carrasco, Maider</au><au>Head, Megan L.</au><au>Jennions, Michael D.</au><au>Priest, Nick</au><au>Priest, Nick</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The effects of male age, sperm age and mating history on ejaculate senescence</atitle><jtitle>Functional ecology</jtitle><date>2019-07</date><risdate>2019</risdate><volume>33</volume><issue>7</issue><spage>1267</spage><epage>1279</epage><pages>1267-1279</pages><issn>0269-8463</issn><issn>1365-2435</issn><eissn>1365-2435</eissn><abstract>In polyandrous species, a male’s reproductive success depends on his ability to fertilize females, which, in turn, depends on his mating ability and his ability to produce competitive ejaculates. In many species, sperm traits differ between old and young males in ways that are likely to decrease the sperm competitiveness and fertility of older males. This age–ejaculate quality relationship is attributed to male ageing (i.e., senescence).
In a natural setting, male age and mating history are usually confounded: older males have usually mated and replenished their sperm supplies more often, so they have made a greater lifetime reproductive effort. In principle, the costs of reproduction, independent of any causal effect of male age, could generate an age‐related decline in ejaculate quality.
To date, only a handful of studies have determined how male age, reproductive effort or their interaction affect ejaculate quality. Here, we experimentally manipulated the long‐term mating history of 209 adult male mosquitofish (Gambusia holbrooki) over 14 weeks (N = 1,118 sperm samples). Males either had direct access to females and could mate freely, or had only visual and olfactory access to females. We documented the effect of mating history, adult male age (3, 9 and 14 weeks post‐maturation) and their interaction on sperm velocity, sperm reserves and the rate of sperm replenishment. For sperm velocity, we additionally examined the effects of sperm age, because when older males mate less (or more) often than younger males there will be a correlation between mean sperm age and male age.
Sexually active males produced fewer sperm and replenished their sperm at a lower rate, and their sperm had lower velocity than males prevented from mating. Though older males produced more sperm, the rate of replenishment and velocity of their sperm was lower than the sperm of younger males. We also tested for a difference in the velocity of recently replenished (<24 hr) and older sperm (i.e., post‐meiotic sperm senescence). There was no evidence that male age or mating history affects the extent of sperm senescence, but older sperm swam faster than recently produced sperm. Crucially, complex interactions are evident between male age and male mating history with respect to sperm number and the proportion of sperm that are replenished.
These results suggest that male age and mating history will interact to determine the reproductive success of a male under sperm competition. They reveal a complex relationship between a male’s age and his ejaculate quality. We suggest that both mating history and sperm age should be controlled for when measuring the intrinsic rate of senescence for male reproductive traits if the goal is to isolate effects that are solely attributable to a male’s chronological age.
A plain language summary is available for this article.
Plain Language Summary</abstract><cop>London</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/1365-2435.13305</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-4349-8163</orcidid><orcidid>https://orcid.org/0000-0002-8123-7661</orcidid><orcidid>https://orcid.org/0000-0001-9221-2788</orcidid><orcidid>https://orcid.org/0000-0003-3442-4189</orcidid><orcidid>https://orcid.org/0000-0003-0349-7967</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Age ageing Aging Aging (natural) Animal reproduction Breeding success Chronology Competitiveness Death benefits Females Fertility Males Mating mating experience Meiosis mosquitofish Replenishment Reproduction Reproductive effort Senescence sexual selection Sperm Sperm competition sperm quality Universal life Velocity |
title | The effects of male age, sperm age and mating history on ejaculate senescence |
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