Skip to main content
Log in

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

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 23:672–675

  • Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex‐biased dispersal. Mol Ecol 21:2092–2105

    Article  PubMed  Google Scholar 

  • 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 14:1789–1801

    Article  CAS  PubMed  Google Scholar 

  • Banks SC, Knight EJ, Dubach JE, Lindenmayer DB (2008) Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums. J Anim Ecol 77:1250–1256

    Article  PubMed  Google Scholar 

  • 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 162:359–370

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using ‘Eigen’ and S4. https://cran.r-project.org/web/packages/lme4/index.html

  • Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511

    Article  Google Scholar 

  • 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 21:572–586

    Article  PubMed  Google Scholar 

  • Blyton MDJ, Lindenmayer DB, Banks SC (2014a) Maternal lineages best explain the associations of a semisocial marsupial. Behav Ecol 25:1212–1222

    Article  Google Scholar 

  • Blyton MDJ, Shaw R, Banks SC (2014b) Development of a powerful microsatellite marker panel for Trichosurus cunninghami. Conserv Genet Resour 6:95–97

    Article  Google Scholar 

  • Blyton MDJ, Banks SC, Peakall R (2015) The effect of sex-biased dispersal on opposite-sexed spatial genetic structure and inbreeding risk. Mol Ecol 24:1681–1695

    Article  PubMed  Google Scholar 

  • Brooker M, Rowley I, Adams M, Baverstock P (1990) Promiscuity: an inbreeding avoidance mechanism in a socially monogamous species? Behav Ecol Sociobiol 26:191–199

    Google Scholar 

  • 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 287–336

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Cockburn A, Scott MP, Scotts DJ (1985) Inbreeding avoidance and male-biased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim Behav 33:908–915

    Article  Google Scholar 

  • 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 137:567–596

  • Daniels SJ, Walters JR (2000) Inbreeding depression and its effects on natal dispersal in red-cockaded woodpeckers. Condor 102:482–491

    Article  Google Scholar 

  • Dewsbury DA (1988) Kin discrimination and reproductive behavior in muroid rodents. Behav Genet 18:525–536

    Article  CAS  PubMed  Google Scholar 

  • 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 15:4555–4567

    Article  CAS  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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 60:272–277

    Article  Google Scholar 

  • Gavish L, Hofmann JE, Getz LL (1984) Sibling recognition in the prairie vole, Microtus ochrogaster. Anim Behav 32:362–366

    Article  Google Scholar 

  • Guillaume F, Perrin N (2009) Inbreeding load, bet hedging, and the evolution of sex‐biased dispersal. Am Nat 173:536–541

    Article  PubMed  Google Scholar 

  • 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 13:3621–3632

    Article  CAS  PubMed  Google Scholar 

  • 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 15:2997–3007

    Article  CAS  PubMed  Google Scholar 

  • Holmes WG, Sherman PW (1983) Kin recognition in animals. Am Sci 71:46–55

    Google Scholar 

  • Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:999–1006

    Article  Google Scholar 

  • Kiørboe T (2008) Optimal swimming strategies in mate-searching pelagic copepods. Oecologia 155:179–192

  • Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467–475

    Article  PubMed  Google Scholar 

  • Krackow S, Matuschak B (1991) Mate choice for non-siblings in wild house mice: evidence from a choice test and a reproductive test. Ethology 88:99–108

    Article  Google Scholar 

  • Lam MKP, Hickson RE, Cowan PE, Cooper DW (2000) A major histocompatibility (MHC) microsatellite locus in brushtail possums (Trichosurus vulpecula). Online J Vet Res 4:139–141

    Google Scholar 

  • Liebgold EB, Brodie ED, Cabe PR (2011) Female philopatry and male‐biased dispersal in a direct‐developing salamander, Plethodon cinereus. Mol Ecol 20:249–257

    Article  PubMed  Google Scholar 

  • 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 23:531–546

    Article  Google Scholar 

  • 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 23:343–362

    Article  Google Scholar 

  • 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 245:1–13

    Article  Google Scholar 

  • 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 50:369–394

    Article  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marshall RC, Buchanan KL, Catchpole CK (2007) Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus. Anim Behav 73:629–635

    Article  Google Scholar 

  • Martin J (2005) Behavioral ecology of the bobuck (Trichosurus cunnunghami). PhD-thesis, The University of Melbourne, Melbourne

  • Martin J, Handasyde K, Taylor A, Coulson G (2007) Long-term pair-bonds without mating fidelity in a mammal. Behaviour 144:1419–1445

    Article  Google Scholar 

  • Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745

    Google Scholar 

  • McCarthy MA, Lindenmayer DB (1998) Population density and movement data for predicting mating systems of arboreal marsupials. Ecol Model 109:193–202

    Article  Google Scholar 

  • Møller AP (1992) Frequency of female copulations with multiple males and sexual selection. Am Nat 139:1089–1101

    Article  Google Scholar 

  • 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–R157

    Article  CAS  PubMed  Google Scholar 

  • 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 61:1075–1079

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Exel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Exel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed Central  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206

    Article  CAS  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • 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 12:1–21

    Article  Google Scholar 

  • 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 272:759–767

    Article  Google Scholar 

  • Rioux-Paquette E, Festa-Bianchet M, Coltman DW (2010) No inbreeding avoidance in an isolated population of bighorn sheep. Anim Behav 80:865–871

  • Robinson SP, Simmons LW, Kennington WJ (2013) Estimating relatedness and inbreeding using molecular markers and pedigrees: the effect of demographic history. Mol Ecol 22:5779–5792

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Schnute J, Boers N, Haigh R (2012) PBSmapping: mapping fisheries data and spatial analysis tools. R package version 2.65.40. https://cran.r-project.org/web/packages/

  • 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 145–154

    Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Stow A, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13:443–447

    Article  CAS  PubMed  Google Scholar 

  • 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 78:778–788

    Article  PubMed  Google Scholar 

  • Taylor AC, Cooper DW (1998) Microsatellite markers for the Phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula). Mol Ecol 7:1780–1782

    Article  CAS  PubMed  Google Scholar 

  • Varian-Ramos CW, Webster MS (2012) Extrapair copulations reduce inbreeding for female red-backed fairy-wrens, Malurus melanocephalus. Anim Behav 83:857–864

    Article  Google Scholar 

  • 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 72:215–216

    Article  CAS  PubMed  Google Scholar 

  • Viggers KL, Lindenmayer DB (2000) A population study of the mountain brushtail possum, Trichosurus caninus, in the central highlands of Victoria. Aust J Zool 48:201–216

    Article  Google Scholar 

  • Walker FM, Sunnucks P, Taylor AC (2008) Evidence for habitat fragmentation altering within‐population processes in wombats. Mol Ecol 17:1674–1684

    Article  PubMed  Google Scholar 

  • Waser PM, De Woody JA (2006) Multiple paternity in a philopatric rodent: the interaction of competition and choice. Behav Ecol 17:971–978

    Article  Google Scholar 

  • Waser PM, Berning ML, Pfeifer A (2012) Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates. Mol Ecol 21:554–561

    Article  PubMed  Google Scholar 

  • Winn BE, Vestal BM (1986) Kin recognition and choice of males by wild female house mice (Mus musculus). J Comp Psychol 100:72–75

    Article  Google Scholar 

  • Winter JW (1980) Tooth wear as an age index in a population of the brush-tailed possum, Trichosurus vulpecula (Kerr). Aust Wild Res 7:359–363

    Article  Google Scholar 

Download references

Acknowledgments

Christine Hayes completed the mitochondrial haplotyping. Richard Blyton, Michelle Johnson, Mark Boorman, Guy Leech, Stephanie Bland, Amelia Coman, Mrinalini Pratap, Lachlan McBurney, and David Blair provided assistance with fieldwork. Funding was provided by the Hermon Slade Foundation (HSF 08–4) and the Australian Research Council (DP 0984876). The comments of three anonymous reviewers contributed extensively to the improvements in the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michaela D. J. Blyton.

Ethics declarations

This study complied with the current laws of Australia, where this study was performed. The work was conducted under ANU Animal Ethics approval B.EEG.01.10.

Additional information

Communicated by A. I. Schulte-Hostedde

Significance statement

Dispersal and mate choice are important behaviors that are closely linked. Sex-biased dispersal is thought to reduce inbreeding risk by separating relatives of the opposite sex. We used spatial genetic analyses in a population of mountain brushtail possums to show that dispersal was insufficient to negate the risk of mating among neighboring relatives. However, population genetic analyses showed the population was not inbred, suggesting kin avoidance in mate choice. We identified a dual mate choice pattern, where possums that were not socially pair-bonded apparently chose mates on the basis of relatedness. By contrast, pair-bonded possums neither favored nor avoided kin as mates. This demonstrates the importance of considering both the post-dispersal arrangement of kin and social context when investigating mating patterns in relation to kinship. Our study design provides a valuable approach for evaluating whether and how a species avoids inbreeding.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 269 kb)

ESM 2

(PDF 28 kb)

ESM 2

(PDF 33 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Blyton, M.D.J., Shaw, R.E., Peakall, R. et al. The role of relatedness in mate choice by an arboreal marsupial in the presence of fine-scale genetic structure. Behav Ecol Sociobiol 70, 313–321 (2016). https://doi.org/10.1007/s00265-015-2049-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-2049-z

Keywords

Navigation