Do pre- and post-copulatory sexually selected traits covary in large herbivores?

BMC Evolutionary Biology

Aurélie Cohas¹  Bernat C López³  Sophie Lardy²  Jean-François Lemaître¹  Mariona Ferrandiz-Rovira¹ 

[1] Laboratoire Biométrie et Biologie Evolutive, Université de Lyon, CNRS, UMR5558, Université Lyon 1, F-69622, Villeurbanne, F-69000 Lyon, France;Groupe Ecologie et conservation des vertébrés, Université d’Angers, Faculté des Sciences, 49045 Angers, France;Universitat Autònoma de Barcelona, Cerdanyola del Vallès, 08193 Catalunya, Spain

关键词: Weapon length;    Sperm competition;    Sexual selection;    Secondary sexual traits;    Post-copulatory competition;    Pre-copulatory competition;   

Others  :  856771
DOI  :  10.1186/1471-2148-14-79

 received in 2014-01-08, accepted in 2014-03-13,  发布年份 2014

【 摘 要 】

Background

In most species, males compete to gain both matings (via pre-copulatory competition) and fertilizations (via post-copulatory competition) to maximize their reproductive success. However, the quantity of resources devoted to sexual traits is finite, and so males are predicted to balance their investment between pre- and post-copulatory expenditure depending on the expected pay-offs that should vary according to mating tactics. In Artiodactyla species, males can invest in weapons such as horns or antlers to increase their mating gains or in testes mass/sperm dimensions to increase their fertilization efficiency. Moreover, it has been suggested that in these species, males with territory defence mating tactic might preferentially increase their investment in post-copulatory traits to increase their fertilization efficiency whereas males with female defence mating tactic might increase their investment in pre-copulatory sexually selected traits to prevent other males from copulating with females. In this study, we thus test the prediction that male’s weapon length (pre-copulatory trait) covaries negatively with relative testes size and/or sperm dimensions (post-copulatory traits) across Artiodactyla using a phylogenetically controlled framework.

Results

Surprisingly no association between weapon length and testes mass is found but a negative association between weapon length and sperm length is evidenced. In addition, neither pre- nor post-copulatory traits were found to be affected by male mating tactics.

Conclusions

We propose several hypotheses that could explain why male ungulates may not balance their reproductive investment between pre- and post-copulatory traits.

【 授权许可】

   
2014 Ferrandiz-Rovira et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Clutton-Brock TH: Sexual selection in males and females. Science 2007, 318:1882-1885.
• [2]Leonard JL, Córdoba-Aguilar A: The Evolution of Primary Sexual Characters in Animals. Oxford: Oxford Univ. Press; 2010.
• [3]Birkhead TR, Møller A: Sperm Competition and Sexual Selection. London: London Academic Press; 1998.
• [4]Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K: Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc R Soc Lond B Biol Sci 2003, 270:633-640.
• [5]Loyau A, Gomez D, Moureau B, Thery M, Hart NS, Saint Jalme M, Bennett ATD, Sorci G: Iridescent structurally based coloration of eyespots correlates with mating success in the peacock. Behav Ecol 2007, 18:1123-1131.
• [6]Parker GA: Sperm competition and the evolution of ejaculates: towards a theory base. In Sperm Competition and Sexual Selection. Edited by Birkhead TR, Møller AP. London: London Academic Press; 1998.
• [7]Pizzari T, Parker GA: Sperm competition and sperm phenotype. In Sperm Biology: An Evolutionary Perspective. Edited by Birkhead TR, Hosken DJ, Pitnick S. London: London Academic Press; 2009.
• [8]Snook RR: Sperm in competition: not playing by the numbers. Trends Ecol Evol 2005, 20:46-53.
• [9]Møller AP: Ejaculate quality, testes size and sperm production in mammals. Funct Ecol 1989, 3:91-96.
• [10]Hosken DJ: Sperm competition in bats. Proc R Soc Lond B Biol Sci 1997, 264:385-392.
• [11]Ramm SA, Parker GA, Stockley P: Sperm competition and the evolution of male reproductive anatomy in rodents. Proc R Soc Lond B Biol Sci 2005, 272:949-955.
• [12]Malo AF, Martinez-Pastor F, Alaks G, Dubach J, Lacy RC: Effects of genetic captive- breeding protocols on sperm quality and fertility in the white-footed mouse. Biol Reprod 2010, 83:540-548.
• [13]Pitnick S: Investment in testes and the cost of making long sperm in Drosophila. Am Nat 1996, 148:57-80.
• [14]Ramm SA, Stockley P: Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol Lett 2010, 6:219-221.
• [15]Zuk M, Kolluru GR: Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 1998, 73:415-438.
• [16]Simmons LW, Roberts B: Bacterial immunity traded for sperm viability in male crickets. Science 2005, 309:2031-2041.
• [17]Garvin JC, Dunn PO, Whittingham LA, Steeber DA, Hasselquist D: Do male ornaments signal immunity in the common yellowthroat? Behav Ecol 2008, 19:54-60.
• [18]Parker GA, Lessells CM, Simmons LW: Sperm competition games: a general model for precopulatory male-male competition. Evolution 2013, 67:95-109.
• [19]Simmons LW, Emlen DJ: Evolutionary trade-off between weapons and testes. Proc Natl Acad Sci U S A 2006, 103:16346-16351.
• [20]Fitzpatrick JL, Almbro M, Gonzalez-Voyer A, Kolm N, Simmons LW: Male contest competition and the coevolution of weaponry and testes in Pinnipeds. Evolution 2012, 66:3595-3604.
• [21]Allen BJ, Levinton JS: Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Funct Ecol 2007, 21:154-161.
• [22]Rowe M, Swaddle JP, Pruett-Jones S, Webster MS: Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren. Anim Behav 2010, 79:1239-1246.
• [23]Bro-Jørgensen J: The intensity of sexual selection predicts weapon size in male bovids. Evolution 2007, 61:1316-1326.
• [24]Bro-Jørgensen J: Intra- and intersexual conflicts and cooperation in the evolution of mating strategies: lessons learnt from ungulates. Evol Biol 2011, 38:28-41.
• [25]Clutton-Brock TH: Mammalian mating systems. Proc R Soc Lond B Biol Sci 1989, 236:339-372.
• [26]Ginsberg JR, Rubenstein DI: Sperm competition and variation in zebra mating-behavior. Behav Ecol Sociobiol 1990, 26:427-434.
• [27]Lemaître J-F, Ramm SA, Barton RA, Stockley P: Sperm competition and brain size evolution in mammals. J Evol Biol 2009, 22:2215-2221.
• [28]Malo AF, Garde JJ, Soler AJ, García AJ, Gomendio M, Roldan ERS: Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 2005, 72:822-829.
• [29]Plard F, Bonenfant C, Gaillard J-M: Revisiting the allometry of antlers among deer species: male-male sexual competition as a driver. Oikos 2011, 120:601-606.
• [30]Gomendio M, Tourmente M, Roldan ERS: Why mammalian lineages respond differently to sexual selection: metabolic rate constrains the evolution of sperm size. Proc R Soc Lond B Biol Sci 2011, 278:3135-3141.
• [31]Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A: The delayed rise of present-day mammals. Nature 2007, 446:507-512.
• [32]Agnarsson I, May-Collado LJ: 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 2008, 48:964-998.
• [33]DeYoung RW, Demarais S, Gonzales RA, Honeycutt RL, Gee KL: Multiple paternity in white-tailed deer Odocoileus virginianus revealed by DNA microsatellites. J Mammal 2002, 83:884-892.
• [34]Tourmente M, Gomendio M, Roldan ERS: Sperm competition and the evolution of sperm design in mammals. BMC Evol Biol 2011, 11:12. BioMed Central Full Text
• [35]Mautz BS, Møller AP, Jennions MD: Do male secondary sexual characters signal ejaculate quality? A meta-analysis. Biol Rev 2013, 88:669-682.
• [36]Pitcher TE, Doucet SM, Beausoleil JMJ, Hanley D: Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. J Fish Biol 2009, 74:1450-1461.
• [37]Chargé R, Jalme MS, Lacroix F, Cadet A, Sorci G: Male health status, signalled courtship display, reveals ejaculate quality and hatching success in a lekking specis. J Anim Ecol 2010, 79:843-850.
• [38]Simmons LW, Fitzpatrick JL: Sperm wars and the evolution of male fertility. Reproduction 2012, 144:519-534.
• [39]Vahed K, Parker DJ: The evolution of large testes: sperm competition or male mating rate? Ethology 2012, 118:107-117.
• [40]Gomendio M, Roldan ERS: Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 2008, 52:439-447.
• [41]Pitnick S, Hosken DJ, Birkhead TR: Sperm morphological diversity. In Sperm Biology: An Evolutionary Perspective. Edited by Birkhead TR, Hosken DJ, Pitnick S. London: London Academic Press; 2009.
• [42]Gage MJG: Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc R Soc Lond B Biol Sci 1995, 261:25-30.
• [43]Owen-Smith N: Mortality rates of male and female kudus: the costs of sexual size dimorphism. J Anim Ecol 1993, 62:428-440.
• [44]Lott DF: Intraspecific Variation in the Social Systems of Wild Vertebrates. Cambridge: Cambridge Univ Press; 1991.
• [45]Shutler D: Sexual selection: when to expect trade-offs. Biol Lett 2011, 7:101-104.
• [46]Harvey PH, Pagel MD: The Comparative Method in Evolutionary Biology. Oxford: Oxford Univ Press; 1991.
• [47]Freckleton RP, Harvey PH, Pagel M: Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 2002, 160:712-726.
• [48]Paradis E, Claude J, Strimmer K: APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
• [49]R Development Core Team: R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2012. ISBN 3-900051-07-0, URL http://www.R-project.org/ webcite
• [50]Nakagawa S, Cuthill IC: Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 2007, 82:591-605.