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Fallow deer polyandry is related to fertilization insurance

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Abstract

Polyandry is widespread, but its adaptive significance is not fully understood. The hypotheses used to explain its persistence have rarely been tested in the wild and particularly for large, long-lived mammals. We investigated polyandry in fallow deer, using female mating and reproduction data gathered over 10 years. Females of this species produce a single offspring (monotocous) and can live to 23 years old. Overall, polyandry was evident in 12 % of females and the long-term, consistent proportion of polyandrous females observed, suggests that monandry and polyandry represent alternative mating strategies. Females were more likely to be polyandrous when their first mate had previously achieved high numbers of matings during the rut or was relatively old. However, polyandry was not related to the following factors: female age, the stage of the rut, the dominance ranks of mates, or the number of daily matings achieved by males. Polyandrous and monandrous multiple-mating females were not more likely than single-mating females to be observed with an offspring during the following year, and there were no significant differences in offspring size between these females. These results provide support for a fertility insurance hypothesis, with females remating if fertilization from the first mating was uncertain due to possible sperm depletion. The potential for different female mating strategies among large, polygynous mammals has generally been overlooked. Our findings highlight the complexity of female reproductive strategies and the possible trade-offs between fertilization success, preferences for high-quality males, and potential costs of polyandry, particularly for monotocous species.

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References

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Asher GW, Barrell GK, Peterson AJ (1986) Hormonal changes around oestrus of farmed fallow deer, Dama dama. J Reprod Fert 78:487–496

    Article  CAS  Google Scholar 

  • Bang A, Deshpande S, Sumana A, Gadagkar R (2010) Choosing an appropriate index to construct dominance hierarchies in animal societies: a comparison of three indices. Anim Behav 79:631–636

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 2.15.0. Available at http://CRAN.R-project.org/package=lme4.

  • Bebié N, McElligott AG (2006) Female aggression in red deer (Cervus elaphus): does it indicate competition for mates? Mamm Biol 71:347–355

    Google Scholar 

  • Bergeron P, Réale D, Humphries MM, Garant D (2011) Evidence of multiple paternity and mate selection for inbreeding avoidance in wild eastern chipmunks. J Evol Biol 24:1685–1694

    Article  PubMed  CAS  Google Scholar 

  • Birgersson B (1998) Male-biased maternal expenditure and associated costs in fallow deer. Behav Ecol Sociobiol 43:87–93

    Article  Google Scholar 

  • Birgersson B, Ekvall K, Temrin H (1991) Allosuckling in fallow deer, Dama dama. Anim Behav 42:326–327

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  • Bowyer R, Rachlow J, Stewart K, Van Ballenberghe V (2011) Vocalizations by Alaskan moose: female incitation of male aggression. Behav Ecol Sociobiol 65:2251–2260

    Article  Google Scholar 

  • Briefer E, Vannoni E, McElligott AG (2010) Quality prevails over identity in the sexually selected vocalisations of an ageing mammal. BMC Biol 8:35

    Article  PubMed  Google Scholar 

  • Bro-Jørgensen J (2002) Overt female mate competition and preference for central males in a lekking antelope. P Natl Acad Sci USA 99:9290–9293

    Article  Google Scholar 

  • Bro-Jørgensen J (2007) Reversed sexual conflict in a promiscuous antelope. Curr Biol 17:2157–2161

    Article  PubMed  Google Scholar 

  • Bro-Jørgensen J (2011) Intra- and intersexual conflicts and cooperation in the evolution of mating strategies: lessons learnt from ungulates. Evol Biol 38:28–41

    Article  Google Scholar 

  • Brooks R, Kemp DJ (2001) Can older males deliver the good genes? Trends Ecol Evol 16:308–313

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35

    Article  Google Scholar 

  • Byers JA, Waits L (2006) Good genes sexual selection in nature. P Natl Acad Sci USA 103:16343–16345

    Article  CAS  Google Scholar 

  • Byers JA, Wiseman PA, Jones L, Roffe TJ (2005) A large cost of female mate sampling in pronghorn. Am Nat 166:661–668

    Article  PubMed  Google Scholar 

  • Carling MD, Avsharian Wiseman P, Byers JA (2003) Microsatellite analysis reveals multiple paternity in a population of wild pronghorn antelopes (Antilocapra americana). J Mammal 84:1237–1243

    Article  Google Scholar 

  • Carranza J, Pérez-González J, Mateos C, Fernández-García JL (2009) Parents’ genetic dissimilarity and offspring sex in a polygynous mammal. Mol Ecol 18:4964–4973

    Article  PubMed  CAS  Google Scholar 

  • Ciuti S, Apollonio, M (2011) Do antlers honestly advertise the phenotypic quality of fallow buck (Dama dama) in a lekking population? Ethology 117:133–144

    Google Scholar 

  • Clutton-Brock TH, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH, Albon SD, Gibson RM, Guinness FE (1979) The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). Anim Behav 27:211–225

    Article  Google Scholar 

  • Collet J, Richardson DS, Worley K, Pizzari T (2012) Sexual selection and the differential effect of polyandry. P Natl Acad Sci USA 109:8641–8645

    Article  CAS  Google Scholar 

  • Cornell SJ, Tregenza T (2007) A new theory for the evolution of polyandry as a means of inbreeding avoidance. Proc R Soc Lond B 274:2873–2879

    Article  Google Scholar 

  • Daly M (1978) The cost of mating. Am Nat 112:771–774

    Article  Google Scholar 

  • Dunn SJ, Clancey E, Waits LP, Byers JA (2012) Genetic evidence of inbreeding avoidance in pronghorn. J Zool 288:119–126

    Article  Google Scholar 

  • Endo A, Doi T (2002) Multiple copulations and post-copulatory guarding in a free-living population of sika deer (Cervus nippon). Ethology 108:739–747

    Article  Google Scholar 

  • Farrell ME (2001) Courtship, multiple mating and reproductive synchrony in female fallow deer (Dama dama). Ph.D. thesis, University College Dublin, Dublin.

  • Farrell ME, Briefer E, Hayden T, McElligott AG (2011) Assortative mating in fallow deer reduces the strength of sexual selection. PLoS One 6:e18533

    Article  PubMed  CAS  Google Scholar 

  • Fedorka KM, Mousseau TA (2002) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64:361–367

    Article  Google Scholar 

  • Firman RC, Simmons LW (2011) Male house mice evolving with post-copulatory sexual selection sire embryos with increased viability. Ecol Lett 15:42–46

    Article  PubMed  Google Scholar 

  • Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444:89–92

    Article  PubMed  CAS  Google Scholar 

  • Gibson RM, Jewell PA (1982) Semen quality, female choice and multiple mating in domestic sheep: a test of Trivers’ sexual competence hypothesis. Behaviour 80:9–31

    Article  Google Scholar 

  • Harty HC (2002) Mate selection by females: sampling tactics and mate choice by female fallow deer (Dama dama L.). Ph.D. thesis, University College Dublin, Dublin

  • Hosken DJ, Stockley P (2003) Benefits of polyandry: a life history perspective. Evol Biol 33:173–194

    Article  Google Scholar 

  • Huchard E, Canale CI, Le Gros C, Perret M, Henry P-Y, Kappeler PM (2012) Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate. Proc R Soc Lond B 279:1371–1379

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  PubMed  CAS  Google Scholar 

  • Johnson SL, Gemmell NJ (2012) Are old males still good males and can females tell the difference? Bioessays 34:609–619

    Article  PubMed  Google Scholar 

  • Klemme I, Eccard JA, Ylönen H (2007) Why do female bank voles, Clethrionomys glareolus, mate multiply? Anim Behav 73:623–628

    Article  Google Scholar 

  • Komers PE, Birgersson B, Ekvall K (1999) Timing of estrus in fallow deer is adjusted to the age of available mates. Am Nat 153:431–436

    Article  Google Scholar 

  • Langbein J, Putman R (1992) Reproductive success of female fallow deer in relation to age and condition. In: Brown RD (ed) The biology of deer. Springer, New York, pp 293–299

    Chapter  Google Scholar 

  • Lord M (2006) Neonatal and maternal behaviour in fallow deer (Dama dama L). Ph.D. thesis, University College Dublin, Dublin

  • Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently? Nature 335:440–441

    Article  Google Scholar 

  • Malo A, Roldan ER, Garde J, Soler A, Vicente J, Gortazar C, Gomendio M (2009) What does testosterone do for red deer males? Proc R Soc Lond B 276:971–980

    Article  CAS  Google Scholar 

  • McElligott AG, Hayden TJ (2000) Lifetime mating success, sexual selection and life history of fallow bucks (Dama dama). Behav Ecol Sociobiol 48:203–210

    Article  Google Scholar 

  • McElligott AG, O’Neill KP, Hayden TJ (1999) Cumulative long-term investment in vocalization and mating success of fallow bucks, Dama dama. Anim Behav 57:1159–1116

    Article  PubMed  Google Scholar 

  • McElligott AG, Gammell MP, Harty HC, Paini DR, Murphy DT, Walsh JT, Hayden TJ (2001) Sexual size dimorphism in fallow deer (Dama dama): do larger, heavier males gain greater mating success? Behav Ecol Sociobiol 49:266–272

    Article  Google Scholar 

  • McElligott AG, Altwegg R, Hayden TJ (2002) Age-specific survival and reproductive probabilities: evidence for senescence in male fallow deer (Dama dama). Proc R Soc Lond B 269:1129–1137

    Article  Google Scholar 

  • McElligott AG, Naulty F, Clarke W, Hayden TJ (2003) The somatic cost of reproduction: what determines reproductive effort in prime-aged fallow bucks? Evol Ecol Res 5:1239–1250

    Google Scholar 

  • Moore N, Kelly P, Cahill J, Hayden T (1995) Mating strategies and mating success of fallow (Dama dama) bucks in a non-lekking population. Behav Ecol Sociobiol 36:91–100

    Article  Google Scholar 

  • Pischedda A, Rice WR (2012) Partitioning sexual selection into its mating success and fertilization success components. P Natl Acad Sci USA 109:2049–2053

    Article  CAS  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion. Nature 409:681–682

    Article  PubMed  CAS  Google Scholar 

  • Say L, Naulty F, Hayden TJ (2003) Genetic and behavioural estimates of reproductive skew in male fallow deer. Mol Ecol 12:2793–2800

    Article  PubMed  CAS  Google Scholar 

  • Slatyer RA, Mautz BS, Backwell PRY, Jennions MD (2012) Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol Rev 87:1–33

    Article  PubMed  Google Scholar 

  • Stopher KV, Nussey DH, Clutton-Brock TH, Guinness F, Morris A, Pemberton JM (2011) The red deer rut revisited: female excursions but no evidence females move to mate with preferred males. Behav Ecol 22:808–818

    Article  Google Scholar 

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21

    Article  Google Scholar 

  • Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73

    Article  PubMed  CAS  Google Scholar 

  • Vannoni E, McElligott AG (2009) Fallow bucks get hoarse: vocal fatigue as a possible signal to conspecifics. Anim Behav 78:3–10

    Article  Google Scholar 

  • Vanpé C, Kjellander P, Gaillard JM, Cosson JF, Galan M, Hewison AJM (2009) Multiple paternity occurs with low frequency in the territorial roe deer, Capreolus capreolus. Biol J Linn Soc 97:128–139

    Article  Google Scholar 

  • Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19:127–134

    Article  PubMed  Google Scholar 

  • Wu L (2009) Mixed effects models for complex data. Chapman and Hall, Boca Raton

    Book  Google Scholar 

  • Yasui Y (1998) The “genetic benefits” of female multiple mating reconsidered. Trends Ecol Evol 13:246–250

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank P. Cullen, D. Doran, H. Harty, N. Moore, F. Naulty, K. Nevin, C. Reynolds, N. Reynolds, K. Tipton, and many other volunteers. Thanks to S. Ciuti, M. Festa-Bianchet, A. Malo, B. Pitcher, K. Ruckstuhl, and the anonymous reviewers for their helpful comments. We thank the staff of Phoenix Park and University College Dublin for their assistance. This work was supported by the Office of Public Works, the Department of Education and Enterprise Ireland to MEF during some of the data collection, and the Swiss National Science Foundation to EFB.

Ethical standards

The work described here complies with the current laws of Ireland.

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The authors declare that they have no conflict of interest.

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Correspondence to Elodie F. Briefer or Alan G. McElligott.

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Communicated by K.E. Ruckstuhl

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Table S1

Number of matings by females and males and number of individuals involved in matings for each age class, over the 10 year study (DOC 43 kb)

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Briefer, E.F., Farrell, M.E., Hayden, T.J. et al. Fallow deer polyandry is related to fertilization insurance. Behav Ecol Sociobiol 67, 657–665 (2013). https://doi.org/10.1007/s00265-013-1485-x

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