Behavioral Ecology and Sociobiology

, Volume 70, Issue 3, pp 313–321 | Cite as

The role of relatedness in mate choice by an arboreal marsupial in the presence of fine-scale genetic structure

  • Michaela D. J. Blyton
  • Robyn E. Shaw
  • Rod Peakall
  • David B. Lindenmayer
  • Sam C. Banks
Original Article


Where dispersal distances are restricted or generations overlap, kin may remain spatially clustered, leading to positive spatial genetic structure and the potential for inbreeding. In such circumstances, post-dispersal behavioral mechanisms may be required if individuals are to avoid mating with kin. Here, we conducted an empirical investigation of mate choice in the presence of fine-scale genetic structure. We assessed the potential for mating among relatives using genetic spatial autocorrelation analysis among adult mountain brushtail possums (Trichosurus cunninghami). There was significant positive spatial genetic structure among opposite-sexed adults (on a scale of 200 m), suggesting that kin remained spatially clustered after dispersal. Despite this, no genetic evidence of inbreeding was found. We assessed whether females may potentially avoid inbreeding: (1) by seeking distant mates and/or (2) by the active avoidance of kin in mate choice. Individuals did not choose distant mates, as 97 % of pairs that mated were separated by <200 m. We identified two distinct patterns of mate choice within the one population. Approximately half of the females sampled were socially monogamous (pair-bonded), and there was no evidence that these individuals chose mates on the basis of genetic dissimilarity. By contrast, the remaining (non-pair-bonded) females were more likely to select genetically dissimilar mates. This dual mate choice pattern demonstrates that the role of genetic relatedness in mate choice can be dependent on social context and dispersal patterns.


Fine-scale genetic structure Inbreeding avoidance Mate choice Trichosurus cunninghami 

Supplementary material

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  1. Alho JS, Teplitsky C, Mills JA, Yarrall JW, Merilä J (2012) No evidence for inbreeding avoidance through active mate choice in red-billed gulls. Behav Ecol 23:672–675Google Scholar
  2. Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex‐biased dispersal. Mol Ecol 21:2092–2105CrossRefPubMedGoogle Scholar
  3. Banks SC, Ward S, Lindenmayer D, Finlayson G, Lawson S, Taylor A (2005) The effects of habitat fragmentation on the social kin structure and mating system of the agile antechinus, Antechinus agilis. Mol Ecol 14:1789–1801CrossRefPubMedGoogle Scholar
  4. Banks SC, Knight EJ, Dubach JE, Lindenmayer DB (2008) Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums. J Anim Ecol 77:1250–1256CrossRefPubMedGoogle Scholar
  5. Banks SC, Dubach J, Viggers KL, Lindenmayer DB (2010) Adult survival and microsatellite diversity in possums: effects of major histocompatibility complex-linked microsatellite diversity but not multilocus inbreeding estimators. Oecologia 162:359–370CrossRefPubMedGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using ‘Eigen’ and S4.
  7. Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511CrossRefGoogle Scholar
  8. Blyton MDJ, Banks SC, Peakall R, Lindenmayer DB (2012) Using probability modelling and genetic parentage assignment to test the role of local mate availability in mating system variation. Mol Ecol 21:572–586CrossRefPubMedGoogle Scholar
  9. Blyton MDJ, Lindenmayer DB, Banks SC (2014a) Maternal lineages best explain the associations of a semisocial marsupial. Behav Ecol 25:1212–1222CrossRefGoogle Scholar
  10. Blyton MDJ, Shaw R, Banks SC (2014b) Development of a powerful microsatellite marker panel for Trichosurus cunninghami. Conserv Genet Resour 6:95–97CrossRefGoogle Scholar
  11. Blyton MDJ, Banks SC, Peakall R (2015) The effect of sex-biased dispersal on opposite-sexed spatial genetic structure and inbreeding risk. Mol Ecol 24:1681–1695CrossRefPubMedGoogle Scholar
  12. Brooker M, Rowley I, Adams M, Baverstock P (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199Google Scholar
  13. Bruford MW, Hanotte O, Brookfield JKY, Burke T (1998) Multilocus and single-locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. IRL Press, Oxford, pp 287–336Google Scholar
  14. Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27CrossRefPubMedGoogle Scholar
  15. Cockburn A, Scott MP, Scotts DJ (1985) Inbreeding avoidance and male-biased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim Behav 33:908–915CrossRefGoogle Scholar
  16. Crowley PH, Travers SE, Linton MC, Cohn SL, Sih A, Sargent RC (1991) Mate density, predation risk, and the seasonal sequence of mate choices: a dynamic game. Am Nat 137:567–596Google Scholar
  17. Daniels SJ, Walters JR (2000) Inbreeding depression and its effects on natal dispersal in red-cockaded woodpeckers. Condor 102:482–491CrossRefGoogle Scholar
  18. Dewsbury DA (1988) Kin discrimination and reproductive behavior in muroid rodents. Behav Genet 18:525–536CrossRefPubMedGoogle Scholar
  19. Foerster K, Valcu M, Johnsen A, Kempenaers B (2006) A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Mol Ecol 15:4555–4567CrossRefPubMedGoogle Scholar
  20. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  21. Gardner MG, Godfrey SS, Fenner A, Donnellan SC, Bull CM (2013) Fine-scale spatial structuring as an inbreeding avoidance mechanism in the social skink Egernia stokesii. Aust J Zool 60:272–277CrossRefGoogle Scholar
  22. Gavish L, Hofmann JE, Getz LL (1984) Sibling recognition in the prairie vole, Microtus ochrogaster. Anim Behav 32:362–366CrossRefGoogle Scholar
  23. Guillaume F, Perrin N (2009) Inbreeding load, bet hedging, and the evolution of sex‐biased dispersal. Am Nat 173:536–541CrossRefPubMedGoogle Scholar
  24. Hazlitt S, Eldridge M, Goldizen A (2004) Fine‐scale spatial genetic correlation analyses reveal strong female philopatry within a brush‐tailed rock‐wallaby colony in southeast Queensland. Mol Ecol 13:3621–3632CrossRefPubMedGoogle Scholar
  25. Hazlitt S, Sigg D, Eldridge M, Goldizen A (2006) Restricted mating dispersal and strong breeding group structure in a mid-sized marsupial mammal (Petrogale penicillata). Mol Ecol 15:2997–3007CrossRefPubMedGoogle Scholar
  26. Holmes WG, Sherman PW (1983) Kin recognition in animals. Am Sci 71:46–55Google Scholar
  27. Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:999–1006CrossRefGoogle Scholar
  28. Kiørboe T (2008) Optimal swimming strategies in mate-searching pelagic copepods. Oecologia 155:179–192Google Scholar
  29. Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467–475CrossRefPubMedGoogle Scholar
  30. Krackow S, Matuschak B (1991) Mate choice for non-siblings in wild house mice: evidence from a choice test and a reproductive test. Ethology 88:99–108CrossRefGoogle Scholar
  31. Lam MKP, Hickson RE, Cowan PE, Cooper DW (2000) A major histocompatibility (MHC) microsatellite locus in brushtail possums (Trichosurus vulpecula). Online J Vet Res 4:139–141Google Scholar
  32. Liebgold EB, Brodie ED, Cabe PR (2011) Female philopatry and male‐biased dispersal in a direct‐developing salamander, Plethodon cinereus. Mol Ecol 20:249–257CrossRefPubMedGoogle Scholar
  33. Lindenmayer DB, Welsh A, Donnelly CF, Cunningham RB (1996a) Use of nest trees by the mountain brushtail possum (Trichosurus caninus) (Phalangeridae: Marsupialia). II. Characteristics of occupied trees. Wildl Res 23:531–546CrossRefGoogle Scholar
  34. Lindenmayer DB, Welsh A, Donnelly CF, Meggs RA (1996b) Use of nest trees by the mountain brushtail possum (Trichosurus caninus) (Phalangeridae: Marsupialia). I. Number of occupied trees and frequency of tree use. Wildl Res 23:343–362CrossRefGoogle Scholar
  35. Lindenmayer DB, Lacy RC, Viggers KL (1998) Modelling survival and capture probabilities of the mountain brushtail possum (Trichosurus caninus) in the forests of south-eastern Australia using trap-recapture data. J Zool 245:1–13CrossRefGoogle Scholar
  36. Lindenmayer DB, Dubach J, Viggers KL (2002) Geographic dimorphism in the mountain brushtail possum (Trichosurus caninus): the case for a new species. Aust J Zool 50:369–394CrossRefGoogle Scholar
  37. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedCentralPubMedGoogle Scholar
  38. Marshall RC, Buchanan KL, Catchpole CK (2007) Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus. Anim Behav 73:629–635CrossRefGoogle Scholar
  39. Martin J (2005) Behavioral ecology of the bobuck (Trichosurus cunnunghami). PhD-thesis, The University of Melbourne, MelbourneGoogle Scholar
  40. Martin J, Handasyde K, Taylor A, Coulson G (2007) Long-term pair-bonds without mating fidelity in a mammal. Behaviour 144:1419–1445CrossRefGoogle Scholar
  41. Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745Google Scholar
  42. McCarthy MA, Lindenmayer DB (1998) Population density and movement data for predicting mating systems of arboreal marsupials. Ecol Model 109:193–202CrossRefGoogle Scholar
  43. Møller AP (1992) Frequency of female copulations with multiple males and sexual selection. Am Nat 139:1089–1101CrossRefGoogle Scholar
  44. Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, Vigilant L (2006) Father-daughter inbreeding avoidance in a wild primate population. Curr Biol 16:R156–R157CrossRefPubMedGoogle Scholar
  45. Parrott ML, Ward SJ, Temple-Smith PD (2007) Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis). Behav Ecol Sociobiol 61:1075–1079CrossRefGoogle Scholar
  46. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Exel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  47. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Exel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentralCrossRefPubMedGoogle Scholar
  48. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58CrossRefPubMedGoogle Scholar
  49. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206CrossRefPubMedGoogle Scholar
  50. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  51. R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Google Scholar
  52. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  53. Regan PC, Levin L, Sprecher S, Christopher FS, Gate R (2000) Partner preferences: what characteristics do men and women desire in their short-term sexual and long-term romantic partners? J Psychol Hum Sex 12:1–21CrossRefGoogle Scholar
  54. Richardson DS, Komdeur J, Burke T, von Schantz T (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc R Soc Lond B 272:759–767CrossRefGoogle Scholar
  55. Rioux-Paquette E, Festa-Bianchet M, Coltman DW (2010) No inbreeding avoidance in an isolated population of bighorn sheep. Anim Behav 80:865–871Google Scholar
  56. Robinson SP, Simmons LW, Kennington WJ (2013) Estimating relatedness and inbreeding using molecular markers and pedigrees: the effect of demographic history. Mol Ecol 22:5779–5792CrossRefPubMedGoogle Scholar
  57. Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  58. Schnute J, Boers N, Haigh R (2012) PBSmapping: mapping fisheries data and spatial analysis tools. R package version 2.65.40.
  59. Seebeck JH, Warneke RM, Baxter BJ (1984) Diet of the Bobuck, Trichosurus caninus (Ogilby) (Marsupialia: Phalangeridae) in a mountain forest in Victoria. In: Smith A, Hume ID (eds) Possums and gliders. Surrey Beatty and Sons Pty Limited, Sydney, pp 145–154Google Scholar
  60. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573CrossRefPubMedGoogle Scholar
  61. Stow A, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13:443–447CrossRefPubMedGoogle Scholar
  62. Szulkin M, Zelazowski P, Nicholson G, Sheldon BC (2009) Inbreeding avoidance under different null models of random mating in the great tit. J Anim Ecol 78:778–788CrossRefPubMedGoogle Scholar
  63. Taylor AC, Cooper DW (1998) Microsatellite markers for the Phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula). Mol Ecol 7:1780–1782CrossRefPubMedGoogle Scholar
  64. Varian-Ramos CW, Webster MS (2012) Extrapair copulations reduce inbreeding for female red-backed fairy-wrens, Malurus melanocephalus. Anim Behav 83:857–864CrossRefGoogle Scholar
  65. Viggers KL, Lindenmayer DB (1995) The use of tiletamine hydrochloride and zolazepam hydrochloride for sedation of the mountain brushtail possun Trichosurus caninus Ogilby (Phalangeridae: Marsupialia). Aust Vet J 72:215–216CrossRefPubMedGoogle Scholar
  66. Viggers KL, Lindenmayer DB (2000) A population study of the mountain brushtail possum, Trichosurus caninus, in the central highlands of Victoria. Aust J Zool 48:201–216CrossRefGoogle Scholar
  67. Walker FM, Sunnucks P, Taylor AC (2008) Evidence for habitat fragmentation altering within‐population processes in wombats. Mol Ecol 17:1674–1684CrossRefPubMedGoogle Scholar
  68. Waser PM, De Woody JA (2006) Multiple paternity in a philopatric rodent: the interaction of competition and choice. Behav Ecol 17:971–978CrossRefGoogle Scholar
  69. Waser PM, Berning ML, Pfeifer A (2012) Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates. Mol Ecol 21:554–561CrossRefPubMedGoogle Scholar
  70. Winn BE, Vestal BM (1986) Kin recognition and choice of males by wild female house mice (Mus musculus). J Comp Psychol 100:72–75CrossRefGoogle Scholar
  71. Winter JW (1980) Tooth wear as an age index in a population of the brush-tailed possum, Trichosurus vulpecula (Kerr). Aust Wild Res 7:359–363CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Michaela D. J. Blyton
    • 1
    • 2
  • Robyn E. Shaw
    • 1
    • 2
  • Rod Peakall
    • 1
  • David B. Lindenmayer
    • 2
  • Sam C. Banks
    • 2
  1. 1.Evolution, Ecology and Genetics, Research School of BiologyThe Australian National UniversityCanberraAustralia
  2. 2.The Fenner School of Environment and SocietyThe Australian National UniversityCanberraAustralia

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