Effect of population density on relationship between pre- and postcopulatory sexual traits

in Animal Biology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Abstract

Sexual selection theory states that the premating (ornaments and armaments) sexual traits should trade off with the postmating (testes and ejaculates) sexual traits, assuming that growing and maintaining these traits is expensive and that total reproductive investments are limited. Male-male competition and sperm competition are predicted to affect how males allocate their finite resources to these traits. Here, we studied relative expenditure on pre- and postmating sexual traits among 82 species for three mammalian orders with varying population density using comparative phylogenetic analysis. The results showed that population density affected sexual size dimorphism (SSD) in both Artiodactyla and Carnivora, but not in Primates. However, relative testis mass and sperm size were not affected by population density. Moreover, we did not find associations between the SSD and testis mass or sperm size in three taxonomic groups. The interspecific relationships between pre- and postcopulatory sexual traits did not change with increased population density. Our findings suggest that population density did not affect variation in the relationship between pre- and postcopulatory sexual traits for these three mammalian orders.

Effect of population density on relationship between pre- and postcopulatory sexual traits

in Animal Biology

Sections

References

AgnarssonI.KuntnerM. & May-ColladoL.J. (2010) Dogs, cats, and kin: a molecular species-level phylogeny of Carnivora. Mol. Phylogenet. Evol.54726-745.

AgnarssonI. & May-ColladoL.J. (2008) The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol. Phylogenet. Evol.48964-985.

AnderssonM. (1994) Sexual Selection. Princeton University PressPrinceton, NJ, USA.

BriskieJ.V.MontgomerieR. & BirkheadT.R. (1997) The evolution of sperm size in birds. Evolution51937-945.

BuzattoB.A.RobertsJ.D. & SimmonsL.W. (2015) Sperm competition and the evolution of precopulatory weapons: increasing male density promotes sperm competition and reduces selection on arm strength in a chorusing frog. Evolution692613-2624.

BuzattoB.A.ThyerE.M.RobertsJ.D. & SimmonsL.W. (2017) Sperm competition and the evolution of precopulatory weapons: testis size and amplexus position, but not arm strength, affect fertilization success in a chorusing frog. Evolution71329-341.

ByrneP.G.RobertsJ.D. & SimmonsL.W. (2002) Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol.15347-355.

ByrneP.G.SimmonsL.W. & RobertsJ.D. (2003) Sperm competition and the evolution of gamete morphology in frogs. Proc. Biol. Sci.2702079-2086.

DarwinC. (1871) The Descent of Man and Selection in Relation to Sex. John MurrayLondon, UK.

DevigiliA.EvansJ.P.Di NisioA. & PilastroA. (2015) Multivariate selection drives concordant patterns of pre- and postcopulatory sexual selection in a livebearing fish. Nat. Commun.68291. DOI:10.1038/ncomms9291.

EmlenS.T. & OringL.W. (1977) Ecology, sexual selection, and the evolution of mating systems. Science197215-223.

EvansJ.P. & Garcia-GonzalezF. (2016) The total opportunity for sexual selection and the integration of pre- and post-mating episodes of sexual selection in a complex world. J. Evol. Biol.292338-2361.

FreckletonR.P.HarveyP.H. & PagelM. (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat.160712-726.

GisinerR.C. (1985) Male territorial and reproductive behavior in the Steller sea lion Eumatopias jubatus. PhD dissertation University of California Santa Cruz CA USA.

Gonzalez-VoyerA.González-SuáarezM.VilaC. & RevillaE. (2017) Larger brain size indirectly increases vulnerability to extinction in mammals. Evolution701364-1375.

HarcourtA.H.HarveyP.H.LarsenS.G. & ShortR.V. (1981) Testis size, body weight and breeding system in primates. Nature29355-57.

HegyiG.GaramszegiL.Z. & EensM. (2008) The roles of ecological factors and sexual selection in the evolution of white wing patches in ducks. Behav. Ecol.191208-1216.

HoskenD.J. (1997) Sperm competition in bats. Proc. Biol. Sci.264385-392.

JinL.YangS.N.LiaoW.B. & LüpoldS. (2016a) Altitude underlies variation in the mating system, somatic condition and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis). Behav. Ecol. Sociobiol.701197-1208.

Jin L.MiZ.P. & LiaoW.B. (2016b) Altitudinal variation in male reproductive investment in a polyandrous frog species (Hyla gongshanensis jingdongensis). Anim. Biol.66289-303.

JosephP.N.EmbertsZ.SassonD.A. & MillerC.W. (1998) Males that drop a sexually selected weapon grow larger testes. Evolution72113-122.

KnellR.J. (2009) Population density and the evolution of male aggression. J. Zool.27883-90.

KokkoH. & RankinD.J. (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos. Trans. R. Soc. Lond. B Biol. Sci.361319-334.

KostyunJ.L. & MoyleL.C. (2017) Multiple strong postmating and intrinsic postzygotic reproductive barriers isolate florally diverse species of Jaltomata (Solanaceae). Evolution711556-1571.

KvarnemoC. & SimmonsL.W. (2013) Polyandry as a mediator of sexual selection before and after mating. Philos. Trans. R. Soc. Lond. B Biol. Sci.36820120042. DOI:10.1098/rstb.2012.0042.

LeBlancM.Festa-BianchetM. & Jorgenson J.T. (2001) Sexual size dimorphism in bighorn sheep (Ovis canadensis): effects of population density. Can. J. Zool.791661-1670.

LemaîtreJ.F.RammS.A.BartonR.A. & StockleyP. (2009) Sperm competition and brain size evolution in mammals. J. Evol. Biol.222215-2221.

LiaoW.B. & LuX. (2011) Proximate mechanisms leading to large male-mating advantage in the Andrew’s toad, Bufo andrewsi. Behaviour1481087-1102.

LiaoW.B.MiZ.P.ZhouC.Q.JinL.LouS.L.HanX. & MaJ. (2011) Relative testis size and mating systems in anurans: large testis in multiple-male mating in foam-nesting frogs. Anim. Biol.61225-238.

LiaoW.B.HuangY.ZhongM.J.ZengY.LuoY. & LüpoldS. (2018) Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation? Evolution724-17.

LüpoldS.TomkinsJ.L.SimmonsL.W. & FitzpatrickJ.L. (2014) Female monopolization mediates the relationship between pre- and postcopulatory sexual traits. Nat. Commun.53184. DOI:10.1038/ncomms4184.

LüpoldS.WistubaJ.DammO.S.RiversJ.W. & BirkheadT.R. (2011) Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality. Reproduction141595-605.

LüpoldS.JinL. & LiaoW.B. (2017) Population density and structure drive differential investment in pre- and postmating sexual traits in frogs. Evolution711686-1699.

LüpoldS.ManierM.K.PuniamoorthyN.SchoffC.StarmerW.T.LuepoldS.H.B.BeloteJ.M. & PitnickS. (2016) How sexual selection can drive the evolution of costly sperm ornamentation. Nature533535-538.

MaiC.L.LiuY.H.JinL.MiZ.P. & LiaoW.B. (2017) Altitudinal variation in somatic condition and reproductive investment of male Yunnan pond frogs (Dianrana pleuraden). Zool. Anz.266189-195.

Marie-OrleachL.JanickeT.VizosoD.B.DavidP. & SchärerL. (2016) Quantifying episodes of sexual selection: insights from a transparent worm with fluorescent sperm. Evolution70314-328.

MarlowB.G. (1975) The comparative behaviour of the Australasian sea lions Neophoca cinerea and Phocarctos hookeri (Pinnipedia: Otariidae). Mammalia39159-230.

McCulloughE.L.BuzattoB.A. & SimmonsL.W. (2018) Population density mediates the interaction between pre- and postmating sexual selection. Evolution72893-905.

McDonaldG.C.SpurginL.G.FairfieldE.A.RichardsonD.S. & PizzariT. (2017) Pre- and postcopulatory sexual selection favor aggressive, young males in polyandrous groups of red junglefowl. Evolution711653-1669.

O’BrienD.M.KatsukiM. & EmlenD.J. (2017) Selection on an extreme weapon in the frog-legged leaf beetle (Sagra femorata). Evolution712584-2598.

OrmeC.D.L.FreckletonR.P.ThomasG.H.PetzoldtT. & FritzS.A. (2012) caper: comparative Analyses of Phylogenetics and Evolution in R. (http://R-Forge.R-project.org/projects/caper/).

PagelM.D. (1992) A method for the analysis of comparative data. J. Theor. Biol.156431-442.

ParkerG.A. & PizzariT. (2010) Sperm competition and ejaculate economics. Biol. Rev.85897-934.

ParkerG.A.LessellsC.M. & SimmonsL.W. (2013) Sperm competition games: a general model for pre-copulatory male-male competition. Evolution6795-109.

ParkerG.A. (1970) Sperm competition and its evolutionary consequences in the insects. Biol. Rev.45526-567.

PerelmanP.JohnsonW.E.RoosC.SeuánezH.N.HorvathJ.E.MoreiraM.A.M.KessingB.PontiusJ.RoelkeM.RumplerY.SchneiderM.P.C.SilvaA.O’BrienS.J. & Pecon-Slattery J. (2011) A molecular phylogeny of living primates. PLoS Genet.7e1001342. DOI:10.1371/journal.pgen.1001342.

Pérez-BarberíaF.J.GordonI.J. & PagelM. (2008) The origins of sexual dimorphism in body size in ungulates. Evolution561276-1285.

Pérez i de LanuzaG.CarreteroM.A. & FontE. (2017) Intensity of male-male competition predicts morph diversity in a color polymorphic lizard. Evolution711832-1840.

R Development Core Team (2016) R: a Language and Environment for Statistical Computing. R Foundation for Statistical ComputingVienna, Austria. http://www.R-project.org.

RammS.A. & SchärerL. (2014) The evolutionary ecology of testicular function: size isn’t everything. Biol. Rev.89874-888.

SamaniP. (2018) Digest: evolution of sperm size and number in external fertilizers. Evolution72211-212.

ShultzA.J. & BurnsK.J. (2017) The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae). Evolution711061-1074.

SimmonsL.W. & Fitzpatrick J.L. (2012) Sperm wars and the evolution of male fertility. Reproduction144519-534.

SimmonsL.W.LüpoldS. & FitzpatrickJ.L. (2017) Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol. Evol.32964-976.

StampsJ.A.LososJ.B. & Andrews R.M. (1997) A comparative study of population density and sexual size dimorphism in lizards. Am. Nat.14964-90.

TangT.LuoY.HuangC.H.LiaoW.B. & HuangW.C. (2018) Variation in somatic condition and testes mass in Feirana quadranus along an altitudinal gradient. Anim. Biol.68277-288.

YuX.ZhongM.J.LiD.Y.JinL.LiaoW.B. & KotrschalA. (2018) Large-brained frogs mature later and live longer. Evolution721174-1183.

ZengY.LouS.L.LiaoW.B. & JehleR. (2014) Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location. BMC Evol. Biol.14104.

ZhaoC.L.LuoY.ZhongM.J.XieF.JiangJ.P.LiD.Y. & LiaoW.B. (2018) The size of cerebellum is positively correlated with geographic distribution range in anurans. Anim. Biol.68309-320.

ZhongM.J.YuX. & LiaoW.B. (2018) A review for life-history traits variation in frogs especially for anurans in China. Asian Herpetol. Res.9165-174.

Figures

  • View in gallery

    Body-mass controlled relationships between population density and sexual size dimorphism for three mammalian orders using PGLS. Values in bold are statistically significant.

  • View in gallery

    Body-mass controlled relationships between population density and testis mass for three mammalian orders using PGLS.

  • View in gallery

    Body-mass controlled relationships between population density and sperm length for three mammalian orders using PGLS.

  • View in gallery

    Body-mass controlled relationships between sexual size dimorphism and testis mass for three mammalian orders using PGLS.

  • View in gallery

    Body-mass controlled relationships between sexual size dimorphism and sperm length for three mammalian orders using PGLS.

  • View in gallery

    No effect of population density on body-mass controlled relationships between sexual size dimorphism and testis mass for three mammalian orders using PGLS.

  • View in gallery

    No effect of population density on body-mass controlled relationships between sexual size dimorphism and sperm length for three mammalian orders using PGLS.

Information

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 32 32 13
Full Text Views 31 31 24
PDF Downloads 6 6 2
EPUB Downloads 0 0 0