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Behavioral Ecology and Sociobiology

, Volume 66, Issue 4, pp 529–537 | Cite as

Are low infidelity rates in feral horses due to infanticide?

  • Meeghan E. GrayEmail author
  • Elissa Z. Cameron
  • Mary M. Peacock
  • David S. Thain
  • Veronica S. Kirchoff
Original Paper

Abstract

A growing number of studies conducted on diverse taxa have shown that extra-pair/group paternity is higher than what would be predicted from behavioral observations alone. While it may be beneficial for females to mate with multiple males, this often results in offspring not sired by the behavioral father, which could influence offspring survival, especially in social mammals. Feral horses (Equus caballus) maintain stable social relationships over several years, usually with one stallion defending a harem band of unrelated mares against other males. Sneak copulations by subordinate males have been observed and mares sometimes change bands, both of which can result in foals sired by males other than the dominant band stallion. We measured female fidelity in free-ranging feral horses in 23 bands, with 51 foals over four foaling seasons and tested offspring paternity against parental behaviors. We used 12 polymorphic microsatellite loci and the program CERVUS 2.0 to determine and exclude potential sires. The majority of mares remained in the band with the sire of their foal resulting in most foals being sired by the band stallion. Most foals that were not sired by the band stallion were born in the year after a round-up and we could not determine if they were the result of band changing or sneak copulations. Foals born into a band without their sire had lower survival rates and mothers were significantly more protective of foals not sired by the band stallion. These findings suggest that band stability increases the reproductive success of mares and support the importance of infanticide risk in equid social structure.

Keywords

Equus caballus Fecal DNA Microsatellites Parental behavior Paternity Wild horse 

Notes

Acknowledgments

We thank Kris Krus from the Nevada Genomics Center for providing fragment analysis and technical support. This research was supported the Nevada Arid Rangeland Initiative NOA15353CG, 110615253BS, 140115253BS, 140215253BS, Hatch Grant 13215353BS, and a research grant from the American Society of Mammalogists. We thank several anonymous referees for valuable criticisms of earlier versions of this manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 40:765–773Google Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedCrossRefGoogle Scholar
  4. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  5. Ashley MC (2000) Feral horses in the desert: population genetics, demography, mating and management. Dissertation, University of Nevada, RenoGoogle Scholar
  6. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  7. Berger J (1986) Wild horses of the Great Basin. University of Chicago Press, ChicagoGoogle Scholar
  8. Blumstein DT (2000) The evolution of infanticide in rodents: a comparative analysis. In: van Schaik CP, Jansen CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 178–197CrossRefGoogle Scholar
  9. Borries C (1997) Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal). Behav Ecol Sociobiol 41:139–150CrossRefGoogle Scholar
  10. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999) DNA analyses support the hypothesis that infanticide in adaptive in langur monkeys. Proc Roy Soc Lond B 266:901–904CrossRefGoogle Scholar
  11. Brauch K, Hodges K, Engelhardt A, Fuhrmann K, Shaw E, Heistermann M (2008) Sex-specific reproductive behaviors and paternity in free-ranging Barbary macaques (Macaca sylvanus). Behav Ecol Sociobiol 62:1453–1466CrossRefGoogle Scholar
  12. Cameron EZ, Linklater WL (2000) Individual mares bias investment in sons and daughters in relation to their condition. Anim Behav 60:359–367PubMedCrossRefGoogle Scholar
  13. Cameron EZ, Linklater WL, Stafford KJ, Minot EO (2003) Social grouping and maternal behaviour in feral horses (Equus caballus): the influence of males on maternal protectiveness. Behav Ecol Sociobiol 53:92–101Google Scholar
  14. Cicirello DM, Wolff JO (1990) The effects of mating on infanticide and pup discrimination in white-footed mice. Behav Ecol Sociobiol 26:275–279CrossRefGoogle Scholar
  15. Cohas A, Yoccoz NG, Allaine D (2007) Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behav Ecol Sociobiol 61:1081–1092CrossRefGoogle Scholar
  16. Collins DA, Busse CD, Goodall J (1984) Infanticide in two populations of savanna baboons. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine, Aldine, pp 193–215Google Scholar
  17. Coulon J, Graziani L, Allaine D, Bel MC, Puderoux S (1995) Infanticide in the Alpine Marmot (Marmota marmota). Ethol Ecol Evol 7:191–194CrossRefGoogle Scholar
  18. Crowell-Davis S, Houpt K (1986) Maternal behavior. Vet Clin N Am-Equine 2:557–571Google Scholar
  19. Daly M (1978) The cost of mating. Am Nat 112:771–774CrossRefGoogle Scholar
  20. Dewsbury DA (1984) Sperm competition in muroid rodents. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 547–571Google Scholar
  21. Dreiss AN, Silva N, Richard M, Moyen F, Théry M, Møller AP, Danchin E (2008) Condition-dependent genetic benefits of extrapair fertilization in female blue tits Cyanistes caeruleus. J Evol Biol 21:1814–1822PubMedCrossRefGoogle Scholar
  22. Duncan PB (1982) Foal killing by stallions. Appl Anim Ethol 8:567–570CrossRefGoogle Scholar
  23. Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73:321–346CrossRefGoogle Scholar
  24. Endo A, Doi T (2002) Multiple copulations and post-copulatory guarding in a free-living population of Sika deer (Cervus nippon). Ethology 108:739–747CrossRefGoogle Scholar
  25. Fairbanks LA, McGuire MT (1987) Mother-infant relationships in vervet monkeys: response to new adult males. Int J Primatol 8:351–366CrossRefGoogle Scholar
  26. Feh C (1990) Long-term paternity data for relation to different aspects of rank for Camargue stallions, Equus caballus. Anim Behav 40:995–996CrossRefGoogle Scholar
  27. Feh C, Munkhtuya B (2008) Male infanticide and paternity analyses in a socially natural herd of Przewalski's horses: sexual selection? Behav Process 78:335–339CrossRefGoogle Scholar
  28. Feist JD, McCullough DR (1975) Reproduction in feral horses. J Reprod Fertil Suppl 23:13–18PubMedGoogle Scholar
  29. Feist JD, McCullough DR (1976) Behavior patterns and communication in feral horses. Z Tierpsychol 41:337–371PubMedCrossRefGoogle Scholar
  30. Frantzen MAJ, Silk JB, Ferguson JWH, Wayne RK, Kohn MH (1998) Empirical evaluation of preservation methods for faecal DNA. Mol Ecol 7:1423–1428PubMedCrossRefGoogle Scholar
  31. Goossens B, Chikhi L, Utami SS, de Ruiter J, Bruford MW (2000) A multi-samples, multi-extracts approach for microsatellite analysis of faecal samples on an arboreal ape. Conserv Genet 1:157–162CrossRefGoogle Scholar
  32. Gray ME (2009) An infanticide attempt by a free-roaming feral stallion (Equus caballus). Biol Lett 5:23–25PubMedCrossRefGoogle Scholar
  33. Heitor F, Vicente L (2008) Maternal care and foal social relationships in a herd of Sorraia horses: influence of maternal rank and experience. Appl Anim Behav Sci 113:189–205CrossRefGoogle Scholar
  34. Hinde RA, Atkinson S (1970) Assessing the roles of social partnership in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. Anim Behav 18:169–176CrossRefGoogle Scholar
  35. Hrdy SB (1979) Infanticide among mammals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40CrossRefGoogle Scholar
  36. Huck M, Löttker P, Böhle U, Heymann EW (2005) Paternity and kinship patterns in polyandrous moustached Tamarins (Saguinus mystax). Am J Phys Anthr 127:449–464CrossRefGoogle Scholar
  37. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  38. Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151PubMedCrossRefGoogle Scholar
  39. Kappeler PM, Schäffler L (2008) The lemur syndrome unresolved: extreme male reproductive skew in sifikas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol 62:1007–1015CrossRefGoogle Scholar
  40. Kaseda Y, Khalil AM (1996) Harem size and reproductive success of stallions in Misaki feral horses. Appl Anim Behav Sci 47:163–173CrossRefGoogle Scholar
  41. Kaseda Y, Khalil AM, Ogawa H (1995) Harem stability and reproductive success in Misaki feral horses. Equine Vet J 27:368–372PubMedCrossRefGoogle Scholar
  42. Klingel H (1979) Social organization of feral horses. J Reprod Fertil Suppl 32:89–95Google Scholar
  43. Linklater WL (2000) Adaptive explanations in socio-ecology: lessons from the Equidae. Biol Rev 75:1–20PubMedCrossRefGoogle Scholar
  44. Linklater WL, Cameron EZ, Minot EO, Stafford KJ (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306PubMedCrossRefGoogle Scholar
  45. Maestripieri D (1995) Assessment of danger to themselves and their infants by rhesus macaques (Macaca mulatta) mothers. J Comp Psychol 109:416–420PubMedCrossRefGoogle Scholar
  46. Marklund S, Ellegren H, Eriksson S, Sandberg K, Andersson L (1994) Parentage testing and linkage analysis in the horse using a set of highly polymorphic microsatellites. Anim Genet 25:19–23PubMedGoogle Scholar
  47. Marshall TC, Slate J, Kruuk L, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  48. McDonnell SM, Haviland JCS (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188CrossRefGoogle Scholar
  49. Miller R (1981) Male aggression, dominance and breeding behavior in Red Desert feral horses. Z Tierpsychol 57:340–351CrossRefGoogle Scholar
  50. Monard A, Duncan P, Boy V (1996) The proximate mechanisms of natal dispersal in female horses. Behaviour 133:1095–1124CrossRefGoogle Scholar
  51. Nakamura M (1998) Multiple mating and cooperative breeding in polygynandrous alpine accentors. II. Male mating tactics. Anim Behav 55:277–289PubMedCrossRefGoogle Scholar
  52. Packer C, Pusey AE (1983) Adaptations of female lions to infanticide by incoming males. Am Nat 121:716–728CrossRefGoogle Scholar
  53. Packer C, Pusey AE (1984) Infanticide in carnivores. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine, New York, pp 31–42Google Scholar
  54. Penzhorn BL (1984) A long-term study of social organization and behavior of Cape mountain zebra Equus zebra zebra. Z Tierpsychol 64:97–146CrossRefGoogle Scholar
  55. Pluháček J, Bartoš L (2000) Male infanticide in captive plains zebra, Equus berchelli. Anim Behav 59:689–694PubMedCrossRefGoogle Scholar
  56. Pluháček J, Bartoš L (2005) Further evidence for male infanticide and feticide in captive plains zebra, Equus burchelli. Folia Zool 54:258–262Google Scholar
  57. Preston BT, Stevenson IR (2001) Dominant rams lose out by sperm depletion. Nature 409:682–683CrossRefGoogle Scholar
  58. Pusey AE, Packer C (1994) Infanticide in lions: consequences and counterstrategies. In: Parmigiani S, vom Saal FS (eds) Infanticide and parental care. Harwood Academic Publishers, Chur, pp 277–299Google Scholar
  59. Ryder OA, Massena R (1988) A case of male infanticide in Equus przewalskii. Appl Anim Behav Sci 21:187–190CrossRefGoogle Scholar
  60. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327PubMedCrossRefGoogle Scholar
  61. Tallmadge RL, Hopman TJ, Schug MD, Aquadro CF, Bowling AT, Murray JD, Caetano AR, Antczak DF (1999) Equine dinucleotide repeat loci COR061-COR080. Anim Genet 30:462–478PubMedGoogle Scholar
  62. Schuelke M (2000) An economic method for the florescent labeling of PCR fragments. Nat Biotechnol 18:233–234PubMedCrossRefGoogle Scholar
  63. Sommer V (1994) Infanticide among the langurs of Jodhpur: testing the sexual selection hypothesis with a long-term record. In: Parmigiani S, vom Saal FS (eds) Infanticide and parental care. Harwood Academic Publishers, Chur, pp 155–198Google Scholar
  64. Stockley P (2003) Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc R Soc Lond B 270:271–278CrossRefGoogle Scholar
  65. Suter SM, Keiser M, Feignoux R, Meyer DR (2007) Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males. Proc R Soc Lond B 274:2865–2872CrossRefGoogle Scholar
  66. Tozaki T, Inoue S, Mashima S, Ohta M, Miura N, Tomita M (2000a) Sequence analysis of trinucleotide repeat microsatellites from an enrichment library of the equine genome. Genome 43:354–565PubMedCrossRefGoogle Scholar
  67. Tozaki T, Kakoi H, Mashima S, Hirota K, Hasegawa T, Ishida N, Miura N, Tomita M (2000b) The isolation and characterization of 18 equine microsatellite loci, TKY272-TKY289. Anim Genet 31:140–157CrossRefGoogle Scholar
  68. Tozaki T, Kakoi H, Mashima S, Hirota K, Hasegawa T, Ishida N, Miura N, Choi-Miura NH, Tomita M (2001) Population study and validation of paternity testing for thoroughbred horses by 15 microsatellite loci. J Vet Med Sci 63:1191–1197PubMedCrossRefGoogle Scholar
  69. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73PubMedCrossRefGoogle Scholar
  70. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  71. Valière N (2002) GIMELT: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379Google Scholar
  72. van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Jansen CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60CrossRefGoogle Scholar
  73. van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proc R Soc Lond B 264:1687–1694CrossRefGoogle Scholar
  74. van Schaik CP, Hodges KK, Nunn CL (2000) Paternity confusion and the ovarian cycle of female primates. In: van Schaik CP, Jansen CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 361–387CrossRefGoogle Scholar
  75. vom Saal FS, Franks P, Boechler M, Palanza M, Parmigiani S (1995) Nest defense and survival of offspring in highly aggressive wild Canadian female house mice. Physiol Behav 58:669–678PubMedCrossRefGoogle Scholar
  76. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256PubMedCrossRefGoogle Scholar
  77. Wedell N (1997) Ejaculate size in bushcrickets: the importance of being large. J Evol Biol 10:315–325CrossRefGoogle Scholar
  78. Wehausen JD, Ramey RR II, Epps CW (2004) Experiments in DNA extraction and PCR amplification from bighorn sheep feces: the importance of DNA extraction method. J Hered 95:503–509PubMedCrossRefGoogle Scholar
  79. Wolff JO (1985) Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus. Anim Behav 33:117–123CrossRefGoogle Scholar
  80. Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Meeghan E. Gray
    • 1
    • 2
    Email author
  • Elissa Z. Cameron
    • 3
  • Mary M. Peacock
    • 2
    • 4
  • David S. Thain
    • 1
  • Veronica S. Kirchoff
    • 4
  1. 1.Department of Agriculture, Nutrition and Veterinary Science, MS 202University of NevadaRenoUSA
  2. 2.Program in Ecology, Evolution and Conservation BiologyUniversity of NevadaRenoUSA
  3. 3.School of ZoologyUniversity of TasmaniaHobartAustralia
  4. 4.Department of Biology, MS 314University of NevadaRenoUSA

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