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.
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References
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 40:765–773
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, Princeton
Ashley MC (2000) Feral horses in the desert: population genetics, demography, mating and management. Dissertation, University of Nevada, Reno
Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368
Berger J (1986) Wild horses of the Great Basin. University of Chicago Press, Chicago
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 178–197
Borries C (1997) Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal). Behav Ecol Sociobiol 41:139–150
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 266:901–904
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 62:1453–1466
Cameron EZ, Linklater WL (2000) Individual mares bias investment in sons and daughters in relation to their condition. Anim Behav 60:359–367
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 53:92–101
Cicirello DM, Wolff JO (1990) The effects of mating on infanticide and pup discrimination in white-footed mice. Behav Ecol Sociobiol 26:275–279
Cohas A, Yoccoz NG, Allaine D (2007) Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behav Ecol Sociobiol 61:1081–1092
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 193–215
Coulon J, Graziani L, Allaine D, Bel MC, Puderoux S (1995) Infanticide in the Alpine Marmot (Marmota marmota). Ethol Ecol Evol 7:191–194
Crowell-Davis S, Houpt K (1986) Maternal behavior. Vet Clin N Am-Equine 2:557–571
Daly M (1978) The cost of mating. Am Nat 112:771–774
Dewsbury DA (1984) Sperm competition in muroid rodents. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 547–571
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 21:1814–1822
Duncan PB (1982) Foal killing by stallions. Appl Anim Ethol 8:567–570
Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73:321–346
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
Fairbanks LA, McGuire MT (1987) Mother-infant relationships in vervet monkeys: response to new adult males. Int J Primatol 8:351–366
Feh C (1990) Long-term paternity data for relation to different aspects of rank for Camargue stallions, Equus caballus. Anim Behav 40:995–996
Feh C, Munkhtuya B (2008) Male infanticide and paternity analyses in a socially natural herd of Przewalski's horses: sexual selection? Behav Process 78:335–339
Feist JD, McCullough DR (1975) Reproduction in feral horses. J Reprod Fertil Suppl 23:13–18
Feist JD, McCullough DR (1976) Behavior patterns and communication in feral horses. Z Tierpsychol 41:337–371
Frantzen MAJ, Silk JB, Ferguson JWH, Wayne RK, Kohn MH (1998) Empirical evaluation of preservation methods for faecal DNA. Mol Ecol 7:1423–1428
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 1:157–162
Gray ME (2009) An infanticide attempt by a free-roaming feral stallion (Equus caballus). Biol Lett 5:23–25
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 113:189–205
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 18:169–176
Hrdy SB (1979) Infanticide among mammals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40
Huck M, Löttker P, Böhle U, Heymann EW (2005) Paternity and kinship patterns in polyandrous moustached Tamarins (Saguinus mystax). Am J Phys Anthr 127:449–464
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Kappeler PM (1997) Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs. Biol Rev 72:111–151
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 62:1007–1015
Kaseda Y, Khalil AM (1996) Harem size and reproductive success of stallions in Misaki feral horses. Appl Anim Behav Sci 47:163–173
Kaseda Y, Khalil AM, Ogawa H (1995) Harem stability and reproductive success in Misaki feral horses. Equine Vet J 27:368–372
Klingel H (1979) Social organization of feral horses. J Reprod Fertil Suppl 32:89–95
Linklater WL (2000) Adaptive explanations in socio-ecology: lessons from the Equidae. Biol Rev 75:1–20
Linklater WL, Cameron EZ, Minot EO, Stafford KJ (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306
Maestripieri D (1995) Assessment of danger to themselves and their infants by rhesus macaques (Macaca mulatta) mothers. J Comp Psychol 109:416–420
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 25:19–23
Marshall TC, Slate J, Kruuk L, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
McDonnell SM, Haviland JCS (1995) Agonistic ethogram of the equid bachelor band. Appl Anim Behav Sci 43:147–188
Miller R (1981) Male aggression, dominance and breeding behavior in Red Desert feral horses. Z Tierpsychol 57:340–351
Monard A, Duncan P, Boy V (1996) The proximate mechanisms of natal dispersal in female horses. Behaviour 133:1095–1124
Nakamura M (1998) Multiple mating and cooperative breeding in polygynandrous alpine accentors. II. Male mating tactics. Anim Behav 55:277–289
Packer C, Pusey AE (1983) Adaptations of female lions to infanticide by incoming males. Am Nat 121:716–728
Packer C, Pusey AE (1984) Infanticide in carnivores. In: Hausfater G, Hrdy SB (eds) Infanticide: comparative and evolutionary perspectives. Aldine, New York, pp 31–42
Penzhorn BL (1984) A long-term study of social organization and behavior of Cape mountain zebra Equus zebra zebra. Z Tierpsychol 64:97–146
Pluháček J, Bartoš L (2000) Male infanticide in captive plains zebra, Equus berchelli. Anim Behav 59:689–694
Pluháček J, Bartoš L (2005) Further evidence for male infanticide and feticide in captive plains zebra, Equus burchelli. Folia Zool 54:258–262
Preston BT, Stevenson IR (2001) Dominant rams lose out by sperm depletion. Nature 409:682–683
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 277–299
Ryder OA, Massena R (1988) A case of male infanticide in Equus przewalskii. Appl Anim Behav Sci 21:187–190
Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327
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 30:462–478
Schuelke M (2000) An economic method for the florescent labeling of PCR fragments. Nat Biotechnol 18:233–234
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 155–198
Stockley P (2003) Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc R Soc Lond B 270:271–278
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 274:2865–2872
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 43:354–565
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 31:140–157
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 63:1191–1197
Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179
Valière N (2002) GIMELT: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379
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 27–60
van Schaik CP, Kappeler PM (1997) Infanticide risk and the evolution of male–female association in primates. Proc R Soc Lond B 264:1687–1694
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 361–387
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 58:669–678
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Wedell N (1997) Ejaculate size in bushcrickets: the importance of being large. J Evol Biol 10:315–325
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 95:503–509
Wolff JO (1985) Maternal aggression as a deterrent to infanticide in Peromyscus leucopus and P. maniculatus. Anim Behav 33:117–123
Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063
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.
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Gray, M.E., Cameron, E.Z., Peacock, M.M. et al. Are low infidelity rates in feral horses due to infanticide?. Behav Ecol Sociobiol 66, 529–537 (2012). https://doi.org/10.1007/s00265-011-1301-4
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DOI: https://doi.org/10.1007/s00265-011-1301-4