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Evolution of extreme-mating behaviour: patterns of extrapair paternity in a species with forced extrapair copulation

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Abstract

Sexual conflict can result in the evolution of extreme mating strategies, including forced copulation. Forced extrapair copulation (FEPC) is generally rare among birds, but is common in re-introduced populations of the hihi (Notiomystis cincta), a socially monogamous, New Zealand endemic, endangered passerine. The aim of this study was to understand the patterns of extrapair paternity in a population where the majority of EPC is forced and to examine the factors, in particular female-specific, influencing the proportion of offspring fathered by extrapair males (EPP—extrapair paternity) and the number of males siring extrapair offspring within a brood (EPM) in this species. Using 8 years of comprehensive paternity, life-history and demographic information for 485 breeding attempts, we show that the frequency of EPP is dependent on (1) social male and female age, (2) the month the female fledged, (3) breeding density and (4) whether it was their first or second reproductive event of the season. In addition, we show that both EPP and EPM are negatively associated with breeding synchrony and clutch size is the most important predictor of EPM. Understanding the drivers of EPP and EPM in species with FECP is important because these are strong determinants of variance in reproductive success and the maintenance of extreme mating behaviour.

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References

  • Adler M (2010) Sexual conflict in waterfowl: why do females resist extrapair copulations? Behav Ecol 21:182–192

    Article  Google Scholar 

  • Armstrong DP, Ewen JG (2001) Testing for food limitation in reintroduced hihi populations: contrasting results for two islands. Pac Conserv Biol 7:87–92

    Google Scholar 

  • Armstrong DP, Davidson RS, Dimond WJ, Perrot JK, Castro I, Ewen JG, Griffiths R, Taylor J (2002) Population dynamics of reintroduced forest birds on New Zealand islands. J Biogeogr 29:609–621

    Article  Google Scholar 

  • Arnqvist G, Kirkpatrick M (2005) The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am Nat 165:26–37

    Article  Google Scholar 

  • Birkhead TR (1998) Sperm competition in birds. Rev Reprod 3:123–129

    Article  PubMed  CAS  Google Scholar 

  • Birkhead TR, Biggins JD (1998) Sperm competition mechanisms in birds: models and data. Behav Ecol 9:253–260

    Article  Google Scholar 

  • Birkhead TR, Hatchwell BJ, Lindner R, Blomqvist D, Pellatt EJ et al (2001) Extrapair paternity in the common murre. Condor 103:158–162

    Article  Google Scholar 

  • Brekke P, Dawson DA, Horsburgh GJ, Ewen JG (2009) Characterization of microsatellite loci in the hihi Notiomystis cincta (Notiomystidae Aves). Mol Ecol Res 9:1255–1258

    Article  CAS  Google Scholar 

  • Brekke P, Bennett PM, Wang J, Pettorelli N, Ewen JG (2010) Sensitive males: inbreeding depression in an endangered bird. Proc R Soc Lond B 277:3677–3684

    Article  Google Scholar 

  • Brekke P, Wang J, Bennett PM, Cassey P, Dawson DA, Horsburgh GJ, Ewen JG (2012) Postcopulatory mechanisms of inbreeding avoidance in the island endemic hihi (Notiomystis cincta). Behav Ecol 23:278–284

    Article  Google Scholar 

  • Brennan PLR, Prum RO (2012) The limits of sexual conflict in the narrow sense: new insights from waterfowl biology. Philos T Roy Soc B 367:2324–2338

    Article  Google Scholar 

  • Brennan PLR, Prum RO, McCracken KG, Sorenson MD, Wilson RE, Birkhead TR (2007) Coevolution of male and female genital morphology in waterfowl. PLoS One 2:e418

    Article  PubMed  Google Scholar 

  • Briskie J, Montgomerie R (2001) Efficient copulation and the evolutionary loss of the avian intromittent organ. J Avian Biol 32:184–187

    Article  Google Scholar 

  • Burg TM, Croxall JP (2006) Extrapair paternities in black-browed Thalassarche melanophris grey-headed T chrysostoma and wandering albatross Diomedea exulans at South Georgia. J Avian Biol 37:331–338

    Article  Google Scholar 

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

    Google Scholar 

  • Castro I, Minot EO, Fordham RA, Birkhead TR (1996) Polygynandry face-to-face copulation and sperm competition in the hihi Notiomystis cincta (Aves: Meliphagidae). Ibis 138:765–771

    Article  Google Scholar 

  • Castro I, Brunton DH, Mason KM, Ebert B, Griffiths R (2003) Life history traits and food supplementation affect productivity in a translocated population of the endangered hihi (stitchbird Notiomystis cincta). Biol Conserv 114:271–280

    Article  Google Scholar 

  • Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365

    Article  Google Scholar 

  • Conrad KF, Johnston PV, Crossman C, Kempenaers B, Robertson RJ, Wheelwright NT, Boag T (2001) High levels of extra-pair paternity in an isolated low-density island population of tree swallows (Tachycineta bicolor). Mol Ecol 10:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Cunningham EJA (2003) Female mate preferences and subsequent resistance to copulation in the mallard. Behav Ecol 14:326–333

    Article  Google Scholar 

  • Dickinson J (2001) Extrapair copulations in western bluebirds (Sialia mexicana): female receptivity favours older males. Behav Ecol Sociobiol 50:423–429

    Article  Google Scholar 

  • Dietrich V, Schmoll T, Winkel W, Epplen J (2004) Pair identity: an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141:817–835

    Article  Google Scholar 

  • Dunn PO, Afton AD, Gloutney ML, Alisauskas RT (1999) Forced copulation results in few extrapair fertilizations in Ross’s and lesser snow geese. Anim Behav 57:1071–1081

    Article  PubMed  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Eliassen S, Kokko H (2008) Current analyses do not resolve whether extra-pair paternity is male or female driven. Behav Ecol Sociobiol 62:1795–1804

    Article  Google Scholar 

  • Ewen JG, Armstrong DP (2000) Male provisioning is negatively correlated with attempted extrapair copulation frequency in the stitchbird (or hihi). Anim Behav 60:429–433

    Article  PubMed  Google Scholar 

  • Ewen JG, Armstrong DP, Lambert D (1999) Floater males gain reproductive success through extrapair fertilizations in the stitchbird. Anim Behav 58:321–328

    Article  PubMed  Google Scholar 

  • Ewen JG, Armstrong DP, Ebert B, Hansen LH (2004) Extra-pair copulation and paternity defence in the hihi (or stitchbird) Notiomystis cincta. New Zeal J Ecol 28:233–240

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, London

    Google Scholar 

  • Genevieve M, Jones W, Techow NMSM, Ryan PG (2012) Dalliances and doubtful dads: what determines extra-pair paternity in socially monogamous wandering albatrosses? Behav Ecol Sociobiol 66:1213–1224

    Article  Google Scholar 

  • Gowaty PA, Buschhaus N (1998) Ultimate causation of aggressive and forced copulation in birds: female resistance, the CODE hypothesis, and social monogamy. Am Zool 38:207–225

    Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • Hill CCE, Gjerdrum C, Elphick CCS (2010) extreme levels of multiple mating characterize the mating system of the saltmarsh sparrow (Ammodramus caudacutus). Auk 127:300–307

    Article  Google Scholar 

  • Hogg JT, Forbes SH (1997) Mating in bighorn sheep: frequent male reproduction via a high-risk “unconventional” tactic. Behav Ecol Sociobiol 41:33–48

    Article  Google Scholar 

  • Hoi H (1997) Assessment of the quality of copulation partners in the monogamous bearded tit. Anim Behav 53:277–286

    Article  Google Scholar 

  • Hoi-Leitner M, Hoi H, Romero-Pujante M, Valera F (1999) Female extra-pair behaviour and environmental quality in the serin (Serinus serinus): a test of the “constrained female hypothesis”. Proc R Soc Lond B 266:1021–1026

    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 K, Burley NT (1997) Mating tactics and mating systems of birds. In: Parker PG, Burley NT (eds) Avian reproductive tactics: female and male perspectives. American Ornithologists’ Union, Washington

    Google Scholar 

  • Jouventin P, Charmantier A, Dubois MP, Jarne P, Bried J (2007) Extra-pair paternity in the strongly monogamous wandering albatross Diomedea exulans has no apparent benefits for females. Ibis 149:67–78

    Article  Google Scholar 

  • Kahn AT, Mautz B, Jennions MD (2010) Females prefer to associate with males with longer intromittent organs in mosquitofish. Biol Lett 6:55–58

    Article  PubMed  Google Scholar 

  • Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Natl Acad Sci USA 101:6530–6535

    Article  PubMed  CAS  Google Scholar 

  • Lessells CM (2006) The evolutionary outcome of sexual conflict. Philos T Roy Soc B 361:301–317

    Article  CAS  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  • Low M (2005a) Female resistance and male force: context and patterns of copulation in the New Zealand stitchbird Notiomystis cincta. J Avian Biol 36:436–448

    Article  Google Scholar 

  • Low M (2005b) The energetic cost of mate guarding is correlated with territorial intrusions in the New Zealand stitchbird. Behav Ecol 17:270–276

    Article  Google Scholar 

  • Low M (2006) Sex, age and season influence morphometrics in the New Zealand stitchbird (or hihi; Notiomystis cincta). Emu 106:297–304

    Article  Google Scholar 

  • Low M, Pärt T (2009) Patterns of mortality for each life-history stage in a population of the endangered New Zealand stitchbird. J Anim Ecol 78:761–771

    Article  PubMed  Google Scholar 

  • Low M, Pärt T, Forslund P (2007) Age-specific variation in reproduction is largely explained by the timing of territory establishment in the New Zealand stitchbird Notiomystis cincta. J Anim Ecol 76:459–470

    Article  PubMed  Google Scholar 

  • Mckinney F, Evarts S (1998) Sexual coercion in waterfowl and other birds. Ornithol Monogr 49:163–195

    Article  Google Scholar 

  • Nicholls JA, Double M, Rowell D, Magrath D (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176

    Article  Google Scholar 

  • Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos T Roy Soc B 361:235–259

    Article  CAS  Google Scholar 

  • Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58

    Article  PubMed  CAS  Google Scholar 

  • Quillfeldt P, Masello JF, Segelbacher G (2012) Extra-pair paternity in seabirds: a review and case study of Thin-billed prions Pachyptila belcheri. J Ornithol 153:367–373

    Article  Google Scholar 

  • Ratti O, Lundberg A, Tegelstrom H, Alatalo RV (2001) No evidence for effects of breeding density and male removal on extrapair paternity in the pied flycatcher. Auk 118:147–155

    Article  Google Scholar 

  • Rowe LD, Ludwig D, Schluter (1994) Time condition and the seasonal decline of avian clutch size. Am Nat 143:698–722

    Article  Google Scholar 

  • Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Stud Behav 22:1–63

    Article  Google Scholar 

  • Spottiswoode C, Møller AP (2004) Extrapair paternity migration and breeding synchrony in birds. Behav Ecol 15:41–57

    Article  Google Scholar 

  • Thiel M, Hinojosa IA (2003) Mating behaviour of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea)—indication for convenience polyandry and cryptic female choice. Behav Ecol Sociobiol 55:11–121

    Article  Google Scholar 

  • Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594

    Article  PubMed  CAS  Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34:365–396

    Article  Google Scholar 

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Acknowledgements

We are grateful to the continuing support of New Zealand’s Department of Conservation and Hihi Recovery Group. We also thank Leila Walker for help with field work. Valuable comments on the manuscript were provided by T. R. Birkhead, P. Brennan and an anonymous reviewer. This work was supported by an AXA Fellowship grant to PB. A Leverhulme Trust Research Grant and NERC MGF Grant to JGE. JGE is supported by a RCUK Fellowship. PC is an ARC Future Fellow (FT0991420).

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Ethical standards

All sampling reported in this article comply with the current laws of New Zealand, the country in which they were performed.

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Correspondence to Patricia Brekke.

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Communicated by D. Rubenstein

Appendix

Appendix

Table 2 Sample sizes per breeding season
Table 3 Sample size for each explanatory variable included in the top model (except clutch number and yearly density shown above)
Table 4 Proportion of extrapair offspring (EPO) per clutch per breeding season

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Brekke, P., Cassey, P., Ariani, C. et al. Evolution of extreme-mating behaviour: patterns of extrapair paternity in a species with forced extrapair copulation. Behav Ecol Sociobiol 67, 963–972 (2013). https://doi.org/10.1007/s00265-013-1522-9

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