The coevolution of male and female genitalia in a mammal: A quantitative genetic insight.
Coevolution
genital morphology
house mouse
os penis
quantitative genetics
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
17
10
2019
revised:
10
04
2020
accepted:
30
05
2020
pubmed:
4
6
2020
medline:
24
3
2021
entrez:
4
6
2020
Statut:
ppublish
Résumé
Male genitalia are among the most phenotypically diverse morphological traits, and sexual selection is widely accepted as being responsible for their evolutionary divergence. Studies of house mice suggest that the shape of the baculum (penis bone) affects male reproductive fitness and experimentally imposed postmating sexual selection has been shown to drive divergence in baculum shape across generations. Much less is known of the morphology of female genitalia and its coevolution with male genitalia. In light of this, we used a paternal half-sibling design to explore patterns of additive genetic variation and covariation underlying baculum shape and female vaginal tract size in house mice (Mus musculus domesticus). We applied a landmark-based morphometrics approach to measure baculum size and shape in males and the length of the vaginal tract and width of the cervix in females. Our results reveal significant additive genetic variation in house mouse baculum morphology and cervix width, as well as evidence for genetic covariation between male and female genital measures. Our data thereby provide novel insight into the potential for the coevolutionary divergence of male and female genital traits in a mammal.
Banques de données
Dryad
['10.5061/dryad.5tb2rbp27']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1558-1567Subventions
Organisme : Australian Research Council
ID : LWS DP 170101315
Pays : International
Informations de copyright
© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.
Références
Ah-King, M., A. B. Barron, and M. E. Herberstein. 2014. Genital evolution: why are females still understudied? PLoS Biol. 12:e1001851.
Åkesson, M., S. Bensch, D. Hasselquist, M. Tarka, and B. Hansson. 2008. Estimating heritabilities and genetic correlations: comparing the “animal mode” with parent-offspring regression using data from a natural population. PLoS One 3:e1739
Allen, E. 1922. The oestrous cycle in the mouse. Am. J. Anat. 30:297-371.
André, G. I., R. C. Firman, and L. W. Simmons. 2018. Phenotypic plasticity in genitalia: baculum shape responds to sperm competition risk in house mice. Proc. R. Soc. B Biol. Sci. 285:20181086.
Arnqvist, G. 2006. Sensory exploitation and sexual conflict. Philos. Trans. R. Soc. B Biol. Sci. 361:375-386.
Arnqvist, G., and L. Rowe. 2002. Antagonistic coevolution between the sexes in a group of insects. Nature 415:787-789.
Arnqvist, G., and L. Rowe 2005. Sexual conflict. Princeton Univ. Press, Princeton, NJ.
Astles, P. A., A. J. Moore, and R. F. Preziosi. 2006. A comparison of methods to estimate cross-environment genetic correlations. J. Evol. Biol. 19:114-122.
Barry, C. M., E. Ji, H. Sharma, L. Beukes, P. I. Vilimas, Y. C. DeGraaf, D. Matusica, and R. V. Haberberger. 2017. Morphological and neurochemical differences in peptidergic nerve fibers of the mouse vagina. J. Comp. Neurol. 525:2394-2410.
Bonet, S., I. Casas, W. V. Holt, and M. Yeste. 2013. Boar reproduction: fundamentals and new biotechnological trends. Springer, Berlin, Heidelberg.
Brennan, P. L. R., and R. O. Prum. 2015. Mechanisms and evidence of genital coevolution: the roles of natural selection, mate choice, and sexual conflict. Cold Spring Harb. Perspect. Biol. 7:1-21.
Brennan, P. L. R., R. O. Prum, K. G. McCracken, M. D. Sorenson, R. E. Wilson, and T. R. Birkhead. 2007. Coevolution of male and female genital morphology in waterfowl. PLoS One 2:e418
Brenner, R. M., and N. B. West. 1975. Hormonal regulation of the reproductive tract in female mammals. Annu. Rev. Physiol. 37:273-302.
Briceño, R. D., and W. G. Eberhard. 2009. Experimental modifications imply a stimulatory function for male tsetse fly genitalia, supporting cryptic female choice theory. J. Evol. Biol. 22:1516-1525.
Brindle, M., and C. Opie. 2016. Postcopulatory sexual selection influences baculum evolution in primates and carnivores. Proc. R. Soc. B Biol. Sci. 283:20161736.
Bronson, F. H. 1979. The reproductive ecology of the house mouse. Q. Rev. Biol. 54:265-299.
Byers, S. L., M. V. Wiles, S. L. Dunn, and R. A. Taft. 2012. Mouse estrous cycle identification tool and images. PLoS One 7:e35538.
Champlin, A. K., D. L. Dorr, and A. H. Gates. 1973. Determining the stage of the estrous cycle in the mouse by the appearance of the vagina. Biol. Reprod. 8:491-494.
Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41-47.
Dougherty, L. R., E. van Lieshout, K. B. McNamara, J. A. Moschilla, G. Arnqvist, and L. W. Simmons. 2017. Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus. Proc. R. Soc. B Biol. Sci. 284:20170132
Eberhard, W. G. 2010. Evolution of genitalia: theories, evidence, and new directions. Genetica 138:5-18.
Eberhard, W. G. 1996. Female control: sexual selection by cryptic female choice. Princeton Univ. Press, Princeton, NJ
Eberhard, W. G. 1985. Sexual selection and animal genitalia. Harvard Univ. Press, Cambridge, MA
Eberhard, W. G., and G. U. C. Lehmann. 2019. Demonstrating sexual selection by cryptic female choice on male genitalia: what is enough? Evolution. 73:2415-2435.
Evans, J. P., E. van Lieshout, and C. Gasparini. 2013. Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia. Proc. R. Soc. B Biol. Sci. 280:20130749-20130749.
Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. 4th ed. Longman, London, U.K.
Firman, R. C., I. Klemme, and L. W. Simmons. 2013. Strategic adjustments in sperm production within and between two island populations of house mice. Evolution 67:3061-3070.
Garcia-Gonzalez, F., L. W. Simmons, J. L. Tomkins, J. S. Kotiaho, and J. P. Evans. 2012. Comparing evolvabilities: common errors surrounding the calculation and use of coefficients of additive genetic variation. Evolution 66:2341-2349.
Garcia-Villar, R., P. L. Toutain, and Y. Ruckebusch. 1982. Electromyographic evaluation of the spontaneous and drug-induced motility of the cervix in sheep. J. Pharmacol. Methods 7:83-90.
Georgas, K. M., J. Armstrong, J. R. Keast, C. E. Larkins, K. M. McHugh, E. M. Southard-Smith, M. J. Cohn, E. Batourina, H. Dan, K. Schneider, et al. 2015. An illustrated anatomical ontology of the developing mouse lower urogenital tract. Development 142:1893-1908.
Giraldi, A., P. Alm, V. Werkström, L. Myllymäki, G. Wagner, and K. E. Andersson. 2002. Morphological and functional characterization of a rat vaginal smooth muscle sphincter. Int. J. Impot. Res. 14:271-282.
Hosken, D. J., and P. Stockley. 2004. Sexual selection and genital evolution. Trends Ecol. Evol. 19:87-93.
Hotzy, C., M. Polak, J. L. Rönn, and G. Arnqvist. 2012. Phenotypic engineering unveils the function of genital morphology. Curr. Biol. 22:2258-2261.
Ilango, K., and R. P. Lane. 2009. Coadaptation of male aedeagal filaments and female spermathecal ducts of the old world phlebotomine sand flies (Diptera: Psychodidae). J. Med. Entomol. 37:653-659.
Kirkpatrick, M., and K. Meyer. 2004. Direct estimation of genetic principal components: simplified analysis of complex phenotypes. Genetics 168:2295-2306.
Kirkpatrick, M., and M. J. Ryan. 1991. The evolution of mating preferences and the paradox of the lek. Nature 350:33-38.
Kotiaho, S. J., R. N. LeBas, M. Puurtinen, and L. J. Tomkins. 2008. On the resolution of the lek paradox. Trends Ecol. Evol. 23:1-3.
Kuntner, M., J. A. Coddington, and J. M. Schneider. 2009. Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution 63:1451-1463.
Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
Mead, L. S., and S. J. Arnold. 2004. Quantitative genetic models of sexual selection. Trends Ecol. Evol. 19:264-271.
Mousseau, T. A., and D. A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181-197.
Orbach, D. N., D. A. Kelly, M. Solano, and P. L. R. Brennan. 2017. Genital interactions during simulated copulation among marine mammals. Proc. R. Soc. B Biol. Sci. 284:1-7.
Parker, G. A. 2006. Sexual conflict over mating and fertilization: an overview. Philos. Trans. R. Soc. B Biol. Sci. 361:235-259.
Pomiankowski, A., and A. P. Moller. 1995. A resolution of the lek paradox. Proc. R. Soc. B Biol. Sci. 260:21-29.
Price, T. D. 2006. Phenotypic plasticity, sexual selection and the evolution of colour patterns. J. Exp. Biol. 209:2368-2376.
Price, T. D., A. Qvarnström, and D. E. Irwin. 2003. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. B Biol. Sci. 270:1433-1440.
Ramm, S. A. 2007. Sexual selection and genital evolution in mammals: a phylogenetic analysis of baculum length. Am. Nat. 169:360-369.
Ramm, S. A., D. A. Edward, A. J. Claydon, D. E. Hammond, P. Brownridge, J. L. Hurst, R. J. Beynon, and P. Stockley. 2015. Sperm competition risk drives plasticity in seminal fluid composition. BMC Biol. 13:87.
Ramm, S. A., L. Khoo, and P. Stockley. 2009. Sexual selection and the rodent baculum: an intraspecific study in the house mouse (Mus musculus domesticus). Genetica 138:129-137.
Ramm, S. A., and P. Stockley. 2009. Adaptive plasticity of mammalian sperm production in response to social experience. Proc. R. Soc. B Biol. Sci. 276:745-751.
Rodriguez, E., D. A. Weiss, J. H. Yang, J. Menshenina, M. Ferretti, T. J. Cunha, D. Barcellos, L. Y. Chan, G. Risbridger, G. R. Cunha, et al. 2011. New insights on the morphology of adult mouse penis. Biol. Reprod. 85:1216-1221.
Roff, D. A. 2002. Life history evolution. Sinauer Associates, Sunderland, MA.
Roff, D. A. 2008. Comparing sire and dam estimates of heritability: jackknife and likelihood approaches. Heredity (Edinb) 100:32-38.
Roff, D. A., and R. Preziosi. 1994. Use of the Jackknife. Society 73:544-548.
Rönn, J., M. Katvala, and G. Arnqvist. 2007. Coevolution between harmful male genitalia and female resistance in seed beetles. Proc. Natl. Acad. Sci. U. S. A. 104:10921-10925.
Rowe, L., and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. B Biol. Sci. 263:1415-1421.
Schultz, N. G., J. Ingels, A. Hillhouse, K. Wardwell, P. L. Chang, J. M. Cheverud, C. Lutz, L. Lu, R. W. Williams, and M. D. Dean. 2016a. The genetic basis of baculum size and shape variation in mice. G3 Genes, Genomes, Genet. 6:1141-1151.
Schultz, N. G., M. Lough-Stevens, E. Abreu, T. Orr, and M. D. Dean. 2016b. The baculum was gained and lost multiple times during mammalian evolution. Integr. Comp. Biol. 56:644-656.
Self, S. G., and K. Y. Liang. 1987. Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J. Am. Stat. Assoc. 82:605-610.
Simmons, L. W. 2014. Sexual selection and genital evolution. Austral Entomol. 53:1-17.
Simmons, L. W., and R. C. Firman. 2014. Experimental evidence for the Evolution of the Mammalian Baculum by Sexual selection. Evolution (N. Y). 68:276-283.
Simmons, L. W., and J. L. Fitzpatrick. 2019. Female genitalia can evolve more rapidly and divergently than male genitalia. Nat. Commun. 10:1312.
Simmons, L. W., and F. Garcia-Gonzalez. 2011. Experimental coevolution of male and female genital morphology. Nat. Commun. 2:374-376.
Sloan, N. S., and L. W. Simmons. 2019. The evolution of female genitalia. J. Evol. Biol. 32:882-899.
Stockley, P. 2012. The baculum. Curr. Biol. 22:1032-1033.
Stockley, P., S. A. Ramm, A. L. Sherborne, M. D. F. Thom, S. Paterson, and J. L. Hurst. 2013. Baculum morphology predicts reproductive success of male house mice under sexual selection. BMC Biol. 11:66.
Tatarnic, N. J., and G. Cassis. 2010. Sexual coevolution in the traumatically inseminating plant bug genus Coridromius. J. Evol. Biol. 23:1321-1326.
Tomkins, J. L., J. Radwan, J. S. Kotiaho, and T. Tregenza. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19:323-328.
van Helden, D. F., A. Kamiya, S. Kelsey, D. R. Laver, P. Jobling, R. Mitsui, and H. Hashitani. 2017. Nerve-induced responses of mouse vaginal smooth muscle. Pflugers Arch. Eur. J. Physiol. 469:1373-1385.
Via, S. 1984. The quantitative genetics of polyphagy in an insect herbivore. II. Genetic correlations in larval performance within and among host plants. Evolution 38:896-905.
Wilson, A. J. 2008. Why h2 does not always equal VA/VP? J. Evol. Biol. 21:647-650.
Zelditch, M. L., D. L. Swiderski, and H. D. Sheets. 2012. Chapter 4: theory of shape. Pp. 75-102 in M. L. Zelditch, D. L. Swiderski, and H. D. Sheets, eds. Geometric morphometrics for biologists. 2nd ed. Academic Press, San Diego, CA.