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

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• 作者：Michaela D. J. Blyton ; Robyn E. Shaw ; Rod Peakall…
• 关键词：Fine ; scale genetic structure ; Inbreeding avoidance ; Mate choice ; Trichosurus cunninghami
• 刊名：Behavioral Ecology and Sociobiology
• 出版年：2016
• 出版时间：March 2016
• 年：2016
• 卷：70
• 期：3
• 页码：313-321
• 全文大小：399 KB
• 参考文献：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 21:2092–2105CrossRef PubMed
  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 14:1789–1801CrossRef PubMed
  Banks SC, Knight EJ, Dubach JE, Lindenmayer DB (2008) Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums. J Anim Ecol 77:1250–1256CrossRef PubMed
  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 162:359–370CrossRef PubMed
  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 18:503–511CrossRef
  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 21:572–586CrossRef PubMed
  Blyton MDJ, Lindenmayer DB, Banks SC (2014a) Maternal lineages best explain the associations of a semisocial marsupial. Behav Ecol 25:1212–1222CrossRef
  Blyton MDJ, Shaw R, Banks SC (2014b) Development of a powerful microsatellite marker panel for Trichosurus cunninghami. Conserv Genet Resour 6:95–97CrossRef
  Blyton MDJ, Banks SC, Peakall R (2015) The effect of sex-biased dispersal on opposite-sexed spatial genetic structure and inbreeding risk. Mol Ecol 24:1681–1695CrossRef PubMed
  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
  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
  Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84:3–27CrossRef PubMed
  Cockburn A, Scott MP, Scotts DJ (1985) Inbreeding avoidance and male-biased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim Behav 33:908–915CrossRef
  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 102:482–491CrossRef
  Dewsbury DA (1988) Kin discrimination and reproductive behavior in muroid rodents. Behav Genet 18:525–536CrossRef PubMed
  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 15:4555–4567CrossRef PubMed
  Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRef
  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 60:272–277CrossRef
  Gavish L, Hofmann JE, Getz LL (1984) Sibling recognition in the prairie vole, Microtus ochrogaster. Anim Behav 32:362–366CrossRef
  Guillaume F, Perrin N (2009) Inbreeding load, bet hedging, and the evolution of sex‐biased dispersal. Am Nat 173:536–541CrossRef PubMed
  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 13:3621–3632CrossRef PubMed
  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 15:2997–3007CrossRef PubMed
  Holmes WG, Sherman PW (1983) Kin recognition in animals. Am Sci 71:46–55
  Kalinowski S, Taper M, Marshall T (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:999–1006CrossRef
  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 60:467–475CrossRef PubMed
  Krackow S, Matuschak B (1991) Mate choice for non-siblings in wild house mice: evidence from a choice test and a reproductive test. Ethology 88:99–108CrossRef
  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
  Liebgold EB, Brodie ED, Cabe PR (2011) Female philopatry and male‐biased dispersal in a direct‐developing salamander, Plethodon cinereus. Mol Ecol 20:249–257CrossRef PubMed
  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 23:531–546CrossRef
  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 23:343–362CrossRef
  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 245:1–13CrossRef
  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 50:369–394CrossRef
  Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedCentral PubMed
  Marshall RC, Buchanan KL, Catchpole CK (2007) Song and female choice for extrapair copulations in the sedge warbler, Acrocephalus schoenobaenus. Anim Behav 73:629–635CrossRef
  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 144:1419–1445CrossRef
  Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745
  McCarthy MA, Lindenmayer DB (1998) Population density and movement data for predicting mating systems of arboreal marsupials. Ecol Model 109:193–202CrossRef
  Møller AP (1992) Frequency of female copulations with multiple males and sexual selection. Am Nat 139:1089–1101CrossRef
  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–R157CrossRef PubMed
  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 61:1075–1079CrossRef
  Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Exel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRef
  Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Exel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentral CrossRef PubMed
  Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58CrossRef PubMed
  Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206CrossRef PubMed
  Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRef
  R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://​www.​r-project.​org/​
  Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
  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 12:1–21CrossRef
  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 272:759–767CrossRef
  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 22:5779–5792CrossRef PubMed
  Rousset F (2008) genepop’007: a complete re‐implementation of the genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRef
  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
  Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573CrossRef PubMed
  Stow A, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol Ecol 13:443–447CrossRef PubMed
  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 78:778–788CrossRef PubMed
  Taylor AC, Cooper DW (1998) Microsatellite markers for the Phalangerid marsupial, the common brushtail possum (Trichosurus vulpecula). Mol Ecol 7:1780–1782CrossRef PubMed
  Varian-Ramos CW, Webster MS (2012) Extrapair copulations reduce inbreeding for female red-backed fairy-wrens, Malurus melanocephalus. Anim Behav 83:857–864CrossRef
  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 72:215–216CrossRef PubMed
  Viggers KL, Lindenmayer DB (2000) A population study of the mountain brushtail possum, Trichosurus caninus, in the central highlands of Victoria. Aust J Zool 48:201–216CrossRef
  Walker FM, Sunnucks P, Taylor AC (2008) Evidence for habitat fragmentation altering within‐population processes in wombats. Mol Ecol 17:1674–1684CrossRef PubMed
  Waser PM, De Woody JA (2006) Multiple paternity in a philopatric rodent: the interaction of competition and choice. Behav Ecol 17:971–978CrossRef
  Waser PM, Berning ML, Pfeifer A (2012) Mechanisms of kin discrimination inferred from pedigrees and the spatial distribution of mates. Mol Ecol 21:554–561CrossRef PubMed
  Winn BE, Vestal BM (1986) Kin recognition and choice of males by wild female house mice (Mus musculus). J Comp Psychol 100:72–75CrossRef
  Winter JW (1980) Tooth wear as an age index in a population of the brush-tailed possum, Trichosurus vulpecula (Kerr). Aust Wild Res 7:359–363CrossRef
  
• 作者单位：Michaela D. J. Blyton (1) (2)
  Robyn E. Shaw (1) (2)
  Rod Peakall (1)
  David B. Lindenmayer (2)
  Sam C. Banks (2)
  
  1. Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT, 2601, Australia
  2. The Fenner School of Environment and Society, The Australian National University, Canberra, ACT, 2601, Australia
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Behavioural Sciences
  Zoology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0762

文摘

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. Keywords Fine-scale genetic structure Inbreeding avoidance Mate choice Trichosurus cunninghami