Behavioral Ecology and Sociobiology

, Volume 70, Issue 12, pp 2139–2147 | Cite as

An experimental test of relatedness-based mate discrimination in a social lizard

  • Genevieve Bordogna
  • George Cunningham
  • Luisa J. Fitzpatrick
  • Ben Halliwell
  • Hannah E. A. MacGregor
  • Kirke L. Munch
  • Erik Wapstra
  • Geoffrey M. While
Original Article

Abstract

One of the major decisions individuals of many species make when deciding who to mate with is whether or not to inbreed. The prevailing theory is that individuals should avoid mating with closely related individuals because of the fitness costs associated with decreased offspring quality. However, theoretical work has suggested that levels of inbreeding depression need to be considerable for these costs to outweigh the possible, kin selected, benefits of inbreeding. While evidence for a preference for inbreeding exists in the literature, empirical results currently lag well behind theory. Here, we conducted an experiment to examine mate discrimination and preference with respect to relatedness in a natural population of the family living lizard, Liopholis whitii. We show that both male and female L. whitii distinguish between related and unrelated individuals and, furthermore, that both sexes preferentially associate with more closely related members of the opposite sex. These results correspond closely with patterns of pairing observed in the wild where both males and females have been shown to choose mating pairs that are more closely related to them than expected by chance. Combined, our findings suggest that mate choice in this system may represent an active preference for mating with related individuals rather than a result of passive constraints associated with population viscosity.

Significance statement

In species with long-term pair bonds, who to pair with is one of the most important decisions an organism will make. Much of the research on this topic focusses on avoiding individuals who are closely related, because mating with closely related individuals (e.g. inbreeding) decreases offspring quality. However, avoiding inbreeding may not always be the optimal strategy; it may actually pay to inbreed under certain conditions. Using a family living lizard that forms long-term pair bonds, we show that males and females preferentially associate with more related potential mates when given a choice. These results add to a growing body of literature which suggests that partner choice with respect to relatedness may be the result of an active preference for more related individuals rather than a result of constraints on optimal partner choice.

Keywords

Inbreeding avoidance Inbreeding preference Mate choice Egernia Kin discrimination 

References

  1. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. doi:10.18637/jss.v067.i01 Google Scholar
  2. Bateson PPG (1982) Preferences for cousins in Japanese quail. Nature 295:236–237CrossRefGoogle Scholar
  3. Bateson P (1983) Optimal outbreeding. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp. 257–277Google Scholar
  4. Bretman A, Newcombe D, Tregenza T (2009) Promiscuous females avoid inbreeding by controlling sperm storage. Mol Ecol 18:3340–3345CrossRefPubMedGoogle Scholar
  5. Bull CM, Cooper SJB (1999) Relatedness and the avoidance of inbreeding in the lizard, Tiliqua Rugosa. Behav Ecol Sociobiol 46:367–372CrossRefGoogle Scholar
  6. Bull CM, Griffin CL, Bonnett M, Gardner MG, Cooper SJB (2001) Discrimination between related and unrelated individuals in the Australian lizard Egernia striolata. Behav Ecol Sociobiol 50:173–179CrossRefGoogle Scholar
  7. Carazo P, Font E, Desfilis E (2011) The role of scent marks in female choice of territories and refuges in a lizard Podarcis hispanica. J Comp Psychol 125:362–365CrossRefPubMedGoogle Scholar
  8. Carazo P, Tan CK, Allen F, Wigby S, Pizzari T (2014) Within-group male relatedness reduces harm to females in Drosophila. Nature 505:672–675CrossRefPubMedGoogle Scholar
  9. Chapple DG (2003) Ecology, life-history, and behavior in the Australian Scincid genus Egernia, with comments on the evolution of complex sociality in lizards. Herpetol Monogr 17:145–180CrossRefGoogle Scholar
  10. Chapple DG, Keogh JS (2005) Complex mating system and dispersal patterns in a social lizard, Egernia whitii. Mol Ecol 14:1215–1227CrossRefPubMedGoogle Scholar
  11. Charlesworth D (2006) Evolution of plant breeding systems. Curr Biol 16:726–735CrossRefGoogle Scholar
  12. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796CrossRefPubMedGoogle Scholar
  13. Duthie AB, Reid JM (2015) What happens after inbreeding avoidance? Inbreeding by rejected relatives and the inclusive fitness benefit of inbreeding avoidance. PLoS One 10:e0125140CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fitzpatrick JL, Evans JP (2014) Postcopulatory inbreeding avoidance in guppies. J Evol Biol 27:2686–2694CrossRefGoogle Scholar
  15. Fitzpatrick LJ, Casparinin C, Fitzpatrick JL, Evans JP (2014) Male-female relatedness and patterns of male reproductive investment in guppies. Biol Lett 10:20140166CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gardner MG, Cooper SJB, Bull CM, Grant WN (1999) Isolation of microsatellite loci from a social lizard, Egernia stokesii, using a modified enrichment procedure. J Hered 90:301–304CrossRefGoogle Scholar
  17. Gardner MG, Bull CM, Cooper SJB, Duffield GA (2001) Genetic evidence for a family structure in stable social aggregations of the Australian lizard Egernia stokesii. Mol Ecol 10:175–183CrossRefPubMedGoogle Scholar
  18. Gardner MG, Sanchez JJ, Dudaniec RY, Rheinberger L, Smith AL, Saint KM (2008) Tiliqua rugosa microsatellites: isolation via enrichment and characterisation of loci for multiplex PCR in T. rugosa and the endangered T. adelaidensis. Conserv Genet 9:233–237CrossRefGoogle Scholar
  19. Griesser M, Halvarsson P, Drobniak SM, Vila C (2015) Fine-scale kin recognition in the absence of social familiarity in the Siberian jay, a monogamous bird species. Mol Ecol 24:5726–5738CrossRefPubMedGoogle Scholar
  20. Grün B, Kosmidis I, Zeileis A (2012) Extended beta regression in R: shaken, stirred, mixed, and partitioned. J Stat Softw. doi:10.18637/jss.v048.i11 Google Scholar
  21. Halliwell B, Uller T, Wapstra E, While GM (2016) Resource distribution mediates social and mating behavior in a family living lizard. Behav Ecol . doi:10.1093/beheco/arw134published onlineGoogle Scholar
  22. Heathcote RJP, Bell E, D’Ettorre P, While GM, Uller T (2014) The scent of sun worship: basking experience alters scent mark composition in male lizards. Behav Ecol Sociobiol 68:861–870CrossRefGoogle Scholar
  23. Heathcote RJP, While GM, McGregor HEA, Sciberras J, Leroy C, D’Ettore P, Uller T (2016) Male behaviour drives assortative reproduction during the initial stages of secondary contact. J Evol Biol 29:1003–1015CrossRefPubMedGoogle Scholar
  24. Hews DK, Date P, Hara E, Castellano MJ (2011) Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulates lizards. Behav Ecol Sociobiol 65:1403–1410CrossRefGoogle Scholar
  25. Keller LF, Arcese P (1998) No evidence for inbreeding avoidancve in a natural population of song sparrows (Melospiza melodia. Am Nat 152:380–392CrossRefPubMedGoogle Scholar
  26. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:19–23Google Scholar
  27. Kleven O, Jacobsen F, Robertson RJ, Lifjeld JT (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467–475CrossRefPubMedGoogle Scholar
  29. Langen K, Schwarzer J, Kullmann H, Bakker TCM, Thünken T (2011) Microsatellite support for active inbreeding in a cichlid fish. PLoS One 6:e24689CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lehtonen J, Kokko H (2015) Why inclusive fitness can make it adaptive to produce less fit extra-pair offspring. Proc R Soc B 282:20142716CrossRefPubMedPubMedCentralGoogle Scholar
  31. Liu X, Ty X, He H, Chen C, Xue F (2014) Evidence for inbreeding depression and pre-copulatory but not post-copulatory inbreeding avoidance in the cabbage beetle Colaphellus bowringi. PLoS One 9:e94389CrossRefPubMedPubMedCentralGoogle Scholar
  32. López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404–406CrossRefPubMedPubMedCentralGoogle Scholar
  33. López P, Martín J (2012) Chemosensory exploration of male scent by female rock lizards result from multiple chemical signals of males. Chem Senses 37:47–54CrossRefPubMedGoogle Scholar
  34. López P, Muñoz A, Martín J (2002) Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 52:342–347CrossRefGoogle Scholar
  35. Main AR, Bull CM (1996) Mother-offspring recognition in two Australian lizards, Tiliqua rugosa and Egernia stokesii. Anim Behav 52:193–200CrossRefGoogle Scholar
  36. Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267:1265–1269CrossRefGoogle Scholar
  37. O’Connor DE, Shine R (2006) Kin discrimination in the social lizard Egernia saxatilis (Scincidae. Behav Ecol 17:206–211CrossRefGoogle Scholar
  38. Oh KP (2011) Inclusive fitness of ‘kissing cousins’: new evidence of a role for kin selection in the evolution of extra-pair mating in birds. Mol Ecol 20:2657–2659CrossRefPubMedGoogle Scholar
  39. Olson LE, Blumstein DT, Pollinger JR, Wayne RK (2012) No evidence for inbreeding avoidance despite demonstrated survival costs in a polygynous rodent. Mol Ecol 21:562–571CrossRefPubMedGoogle Scholar
  40. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp. 123–166CrossRefGoogle Scholar
  41. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Phil Trans R Soc B 361:235–259Google Scholar
  42. Pernatta AP, Reading CJ, Allen JA (2009) Chemoreception and kin discrimination by neonate smooth snakes, Coronella austriaca. Anim Behav 77:363–368CrossRefGoogle Scholar
  43. Pizzari T, Lovlie H, Cornwallis CK (2004) Sex-specific counteracting responses to inbreeding in a bird. Proc R Soc Lond B 271:2115–2121CrossRefGoogle Scholar
  44. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206CrossRefPubMedGoogle Scholar
  45. Puurtinen M (2011) Mate choice for optimal (k)inbreeding. Evolution 65:1501–1505CrossRefPubMedGoogle Scholar
  46. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  47. R Development Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  48. Reid JM, Arcese P, Bocedi G, Duthie AB, Wolak ME, Keller LF (2015) Resolving the conundrum of inbreeding depression but no inbreeding avoidance: estimating sex-specific selection on inbreeding by song sparrows (Melospiza melodia). Evolution 69:2846–2861CrossRefPubMedPubMedCentralGoogle Scholar
  49. Robinson SP, Kennington WJ, Simmons LW (2012) Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster. J Evol Biol 25:716–725CrossRefPubMedGoogle Scholar
  50. Scott M, Llewelyn J, Higgie M, Hoskin C, Pike K, Phillips B (2015) Chemoreception and mating behaviour of a tropical Australian skink. Acta Ethol 18:289–293CrossRefGoogle Scholar
  51. Smith RH (1979) On selection for inbreeding in polygynous animals. Heredity 43:205–211CrossRefGoogle Scholar
  52. Stow AJ, Sunnocks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghamii) in natural and fragmented habitat. Mol Ecol 13:443–447CrossRefPubMedGoogle Scholar
  53. Szulkin M, Stopher KV, Pemberton J, Reid JM (2013) Inbreeding avoidance, tolerance, or preference in animals. Trends Ecol Evol 28:205–211CrossRefPubMedGoogle Scholar
  54. Thünken T, Bakker TCM, Baldauf SA, Kullmann H (2007) Active inbreeding in a cichlid fish and its adaptive significance. Curr Biol 17:225–229CrossRefPubMedGoogle Scholar
  55. Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145CrossRefPubMedGoogle Scholar
  56. Wang C, Lu X (2011) Female ground tits prefer relatives as extra-pair partners: driven by sexual selection? Mol Ecol 20:2851–2863CrossRefPubMedGoogle Scholar
  57. Waser PM, Austad SN, Keane B (1986) When should animals tolerate inbreeding? Am Nat 128:529–537CrossRefGoogle Scholar
  58. While GM, Uller T, Wapstra E (2009a) Variation in social strategies characterise the social and mating system of an Australian lizard, Egernia whitii. Aust Ecol 34:938–949CrossRefGoogle Scholar
  59. While GM, Uller T, Wapstra E (2009b) Family conflict and the evolution of sociality in a non-avian vertebrate. Behav Ecol 20:245–250CrossRefGoogle Scholar
  60. While GM, Uller T, Wapstra E (2011) Variation in social organisation influences the opportunity for sexual selection in a social lizard. Mol Ecol 20:844–852CrossRefPubMedGoogle Scholar
  61. While GM, Uller T, Bordogna G, Wapstra E (2014) Promiscuity resolves constraints on social mate choice imposed by population viscosity. Mol Ecol 23:721–732CrossRefPubMedGoogle Scholar
  62. While GM, Chapple DG, Gardner MG, Uller T, Whiting MJ (2015) Egernia lizards. Curr Biol 25:593–595CrossRefGoogle Scholar
  63. Wolak ME, Reid JM (2016) Is pairing with a relative heritable? Estimating female and male genetic contributions to the degree of biparental inbreeding in song sparrows (Melospiza melodia. Am Nat 187:736–752CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Genevieve Bordogna
    • 1
    • 2
  • George Cunningham
    • 1
  • Luisa J. Fitzpatrick
    • 1
  • Ben Halliwell
    • 1
  • Hannah E. A. MacGregor
    • 1
  • Kirke L. Munch
    • 1
  • Erik Wapstra
    • 1
  • Geoffrey M. While
    • 1
  1. 1.School of Biological SciencesUniversity of TasmaniaHobartAustralia
  2. 2.Global Engagement ServicesSlippery Rock UniversitySlippery RockUSA

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