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Meta-analytic evidence that animals rarely avoid inbreeding

Nature Ecology & Evolution volume 5, pages 949–964 (2021)Cite this article

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Abstract

Animals are usually expected to avoid mating with relatives (kin avoidance) as incestuous mating can lead to the expression of inbreeding depression. Yet, theoretical models predict that unbiased mating with regards to kinship should be common, and that under some conditions, the inclusive fitness benefits associated with inbreeding can even lead to a preference for mating with kin. This mismatch between empirical and theoretical expectations generates uncertainty as to the prevalence of inbreeding avoidance in animals. Here, we synthesized 677 effect sizes from 139 experimental studies of mate choice for kin versus non-kin in diploid animals, representing 40 years of research, using a meta-analytical approach. Our meta-analysis revealed little support for the widely held view that animals avoid mating with kin, despite clear evidence of publication bias. Instead, unbiased mating with regards to kinship appears widespread across animals and experimental conditions. The significance of a variety of moderators was explored using meta-regressions, revealing that the degree of relatedness and prior experience with kin explained some variation in the effect sizes. Yet, we found no difference in kin avoidance between males and females, choice and no-choice experiments, mated and virgin animals or between humans and animals. Our findings highlight the need to rethink the widely held view that inbreeding avoidance is a given in experimental studies.

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Fig. 1: Funnel plot of effect sizes to assess publication bias in the dataset.
Fig. 2: Meta-analytical means for different subsets of the dataset.
Fig. 3: The effect of relatedness and previous experience with kin on effect size estimates.

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Data availability

The datasets generated and analysed during the current study are available at the OSF platform under the following identifier: https://osf.io/e34s9/.

Code availability

The R code used to analyse the data in the current study is available at the OSF platform under the following identifier: https://osf.io/e34s9.

References

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

    PubMed  Google Scholar 

  2. Blouin, S. F. & Blouin, M. Inbreeding avoidance behaviors. Trends Ecol. Evol. 3, 230–233 (1988).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  4. Keller, L. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241 (2002).

    Article  Google Scholar 

  5. Szulkin, M., Stopher, K. V., Pemberton, J. M. & Reid, J. M. Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol. Evol. 28, 205–211 (2013).

    Article  PubMed  Google Scholar 

  6. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, 1998).

  7. Charlesworth, D. & Willis, J. H. The genetics of inbreeding depression. Nat. Rev. Genet. 10, 783–796 (2009).

    Article  CAS  PubMed  Google Scholar 

  8. Parker, G. A. in Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. A.) 123–166 (Academic, 1979).

  9. Duthie, A. B. & Reid, J. M. Evolution of inbreeding avoidance and inbreeding preference through mate choice among interacting relatives. Am. Nat. 188, 651–667 (2016).

    Article  PubMed  Google Scholar 

  10. Lehmann, L. & Perrin, N. Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am. Nat. 162, 638–652 (2003).

    Article  PubMed  Google Scholar 

  11. Kokko, H. Give one species the task to come up with a theory that spans them all: what good can come out of that? Proc. Biol. Sci. 284, 20171652 (2017).

    PubMed  PubMed Central  Google Scholar 

  12. Parker, G. A. Sexual conflict over mating and fertilization: an overview. Philos. Trans. R. Soc. Lond. B 361, 235–259 (2006).

    Article  CAS  Google Scholar 

  13. Ihle, M. & Forstmeier, W. Revisiting the evidence for inbreeding avoidance in zebra finches. Behav. Ecol. 24, 1356–1362 (2013).

    Article  Google Scholar 

  14. Annavi, G. et al. Heterozygosity–fitness correlations in a wild mammal population: accounting for parental and environmental effects. Ecol. Evol. 4, 2594–2609 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Arct, A., Drobniak, S. M. & Cichoń, M. Genetic similarity between mates predicts extrapair paternity—a meta-analysis of bird studies. Behav. Ecol. 26, 959–968 (2015).

    Article  Google Scholar 

  16. Winternitz, J., Abbate, J. L., Huchard, E., Havlicek, J. & Garamszegi, L. Z. Patterns of MHC-dependent mate selection in humans and nonhuman primates: a meta-analysis. Mol. Ecol. 26, 668–688 (2017).

    Article  CAS  PubMed  Google Scholar 

  17. Havlíček, J., Winternitz, J. & Roberts, S. C. Major histocompatibility complex-associated odour preferences and human mate choice: near and far horizons. Philos. Trans. R. Soc. Lond. B 375, 20190260 (2020).

    Article  Google Scholar 

  18. Lizé, A., McKay, R. & Lewis, Z. Kin recognition in Drosophila: the importance of ecology and gut microbiota. ISME J. 8, 469–477 (2014).

    Article  PubMed  Google Scholar 

  19. Heys, C. et al. Evidence that the microbiota counteracts male outbreeding strategy by inhibiting sexual signaling in females. Front. Ecol. Evol. 6, https://doi.org/10.3389/fevo.2018.00029 (2018)

  20. Ala-Honkola, O., Manier, M. K., Lupold, S. & Pitnick, S. No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster. Evolution 65, 2699–2705 (2011).

    Article  PubMed  Google Scholar 

  21. Mack, P. D., Hammock, B. A. & Promislow, D. E. Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt. Evolution 56, 1789–1795 (2002).

    PubMed  Google Scholar 

  22. Loyau, A., Cornuau, J. H., Clobert, J. & Danchin, E. Incestuous sisters: mate preference for brothers over unrelated males in Drosophila melanogaster. PLoS ONE 7, e51293 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tan, C. K. W., Løvlie, H., Pizzari, T. & Wigby, S. No evidence for precopulatory inbreeding avoidance in Drosophila melanogaster. Anim. Behav. 83, 1433–1441 (2012).

    Article  Google Scholar 

  24. Robinson, S. P., Kennington, W. J. & Simmons, L. W. Preference for related mates in the fruit fly, Drosophila melanogaster. Anim. Behav. 84, 1169–1176 (2012).

    Article  Google Scholar 

  25. Ala-Honkola, O., Veltsos, P., Anderson, H. & Ritchie, M. G. Copulation duration, but not paternity share, potentially mediates inbreeding avoidance in Drosophila montana. Behav. Ecol. Sociobiol. 68, 2013–2021 (2014).

    Article  Google Scholar 

  26. Nakamura, S. Inbreeding and rotational breeding of the parasitoid fly, Exorista japonica (Diptera: Tachinidae), for successive rearing. Appl. Entomol. Zool. 31, 433–441 (1996).

    Article  Google Scholar 

  27. Aluja, M., Rull, J., Perez-Staples, D., Diaz-Fleischer, F. & Sivinski, J. Random mating among Anastrepha ludens (Diptera: Tephritidae) adults of geographically distant and ecologically distinct populations in Mexico. Bull. Entomol. Res. 99, 207–214 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Fischer, K. et al. Kin recognition and inbreeding avoidance in a butterfly. Ethology 121, 977–984 (2015).

    Article  Google Scholar 

  29. Mongue, A. J., Ahmed, M. Z., Tsai, M. V. & de Roode, J. C. Testing for cryptic female choice in monarch butterflies. Behav. Ecol. 26, 386–395 (2014).

    Article  Google Scholar 

  30. Haikola, S., Singer, M. C. & Pen, I. Has inbreeding depression led to avoidance of sib mating in the Glanville fritillary butterfly (Melitaea cinxia)? Evol. Ecol. 18, 113–120 (2004).

    Article  Google Scholar 

  31. Välimäki, P., Kivelä, S. M. & Mäenpää, M. I. Mating with a kin decreases female remating interval: a possible example of inbreeding avoidance. Behav. Ecol. Sociobiol. 65, 2037–2047 (2011).

    Article  Google Scholar 

  32. Lewis, Z. & Wedell, N. Male moths reduce sperm investment in relatives. Anim. Behav. 77, 1547–1550 (2009).

    Article  Google Scholar 

  33. Harano, T. & Katsuki, M. Female seed beetles, Callosobruchus chinensis, remate more readily after mating with relatives. Anim. Behav. 83, 1007–1010 (2012).

    Article  Google Scholar 

  34. Edvardsson, M., Rodríguez-Muñoz, R. & Tregenza, T. No evidence that female bruchid beetles, Callosobruchus maculatus, use remating to reduce costs of inbreeding. Anim. Behav. 75, 1519–1524 (2008).

    Article  Google Scholar 

  35. Müller, T. & Müller, C. Consequences of mating with siblings and nonsiblings on the reproductive success in a leaf beetle. Ecol. Evol. 6, 3185–3197 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kuriwada, T., Kumano, N., Shiromoto, K. & Haraguchi, D. Inbreeding avoidance or tolerance? Comparison of mating behavior between mass-reared and wild strains of the sweet potato weevil. Behav. Ecol. Sociobiol. 65, 1483–1489 (2011).

    Article  Google Scholar 

  37. Kuriwada, T., Kumano, N., Shiromoto, K. & Haraguchi, D. The effect of inbreeding on mating behaviour of West Indian sweet potato weevil Euscepes postfasciatus. Ethology 117, 822–828 (2011).

    Article  Google Scholar 

  38. Tyler, F. & Tregenza, T. Why do so many flour beetle copulations fail? Entomol. Exp. Appl. 146, 199–206 (2013).

    Article  Google Scholar 

  39. Mattey, S. N., Smiseth, P. T. & Herberstein, M. No inbreeding avoidance by female burying beetles regardless of whether they encounter males simultaneously or sequentially. Ethology 121, 1031–1038 (2015).

    Article  Google Scholar 

  40. De Luca, P. A. & Cocroft, R. B. The effects of age and relatedness on mating patterns in thornbug treehoppers: inbreeding avoidance or inbreeding tolerance? Behav. Ecol. Sociobiol. 62, 1869–1875 (2008).

    Article  Google Scholar 

  41. Poderoso, J. C. M. et al. Mating preferences and consequences of choosing sibling or non-sibling mates by females of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Fla. Entomol. 96, 419–423 (2013).

    Article  Google Scholar 

  42. Huang, M. H. & Caillaud, M. C. Inbreeding avoidance by recognition of close kin in the pea aphid, Acyrthosiphon pisum. J. Insect Sci. 12, 39 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Stockley, P. Sperm selection and genetic incompatibility: does relatedness of mates affect male success in sperm competition? Proc. R. Soc. Biol. Sci. Ser. B 266, 1663–1669 (1999).

    Article  Google Scholar 

  44. Weddle, C. B. et al. Cuticular hydrocarbons as a basis for chemosensory self-referencing in crickets: a potentially universal mechanism facilitating polyandry in insects. Ecol. Lett. 16, 346–353 (2013).

    Article  PubMed  Google Scholar 

  45. Simmons, L. M. Female choice and the relatedness of mates in the field cricket, Gryllus bimaculatus. Anim. Behav. 41, 493–501 (1991).

    Article  Google Scholar 

  46. Bretman, A., Newcombe, D. & Tregenza, T. Promiscuous females avoid inbreeding by controlling sperm storage. Mol. Ecol. 18, 3340–3345 (2009).

    Article  PubMed  Google Scholar 

  47. Bretman, A., Wedell, N. & Tregenza, T. Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc. Biol. Sci. 271, 159–164 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Simmons, L. W. Kin recognition and its influence on mating preferences of the field cricket, Gryllus bimaculatus (de Geer). Anim. Behav. 38, 68–77 (1989).

    Article  Google Scholar 

  49. Simmons, L. W., Beveridge, M., Wedell, N. & Tregenza, T. Postcopulatory inbreeding avoidance by female crickets only revealed by molecular markers. Mol. Ecol. 15, 3817–3824 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. Simmons, L. W. & Thomas, M. L. No postcopulatory response to inbreeding by male crickets. Biol. Lett. 4, 183–185 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tuni, C., Beveridge, M. & Simmons, L. W. Female crickets assess relatedness during mate guarding and bias storage of sperm towards unrelated males. J. Evol. Biol. 26, 1261–1268 (2013).

    Article  CAS  PubMed  Google Scholar 

  52. Haneke-Reinders, M., Reinhold, K. & Schmoll, T. Sex-specific repeatabilities and effects of relatedness and mating status on copulation duration in an acridid grasshopper. Ecol. Evol. 7, 3414–3424 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Teng, Z. Q. & Kang, L. Egg-hatching benefits gained by polyandrous female locusts are not due to the fertilization advantage of nonsibling males. Evolution 61, 470–476 (2007).

    Article  PubMed  Google Scholar 

  54. Bouchebti, S., Durier, V., Pasquaretta, C., Rivault, C. & Lihoreau, M. Subsocial cockroaches Nauphoeta cinerea mate indiscriminately with kin despite high costs of inbreeding. PLoS ONE 11, e0162548 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lihoreau, M. & Rivault, C. German cockroach males maximize their inclusive fitness by avoiding mating with kin. Anim. Behav. 80, 303–309 (2010).

    Article  Google Scholar 

  56. Lihoreau, M., Zimmer, C. & Rivault, C. Kin recognition and incest avoidance in a group-living insect. Behav. Ecol. 18, 880–887 (2007).

    Article  Google Scholar 

  57. Lihoreau, M., Zimmer, C. & Rivault, C. Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS ONE 3, e3365 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Hedlund, K., Ek, H., Gunnarsson, T. & Svegborn, C. Mate choice and male competition in Orchesella cincta (Collembola). Experientia 46, 524–526 (1990).

    Article  Google Scholar 

  59. Palmer, C. A. & Edmands, S. Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicus. Mar. Biol. 136, 693–698 (2000).

    Article  Google Scholar 

  60. Winsor, G. L. & Innes, D. J. Sexual reproduction in Daphnia pulex (Crustacea: Cladocera): observations on male mating behaviour and avoidance of inbreeding. Freshwat. Biol. 47, 441–450 (2002).

    Article  Google Scholar 

  61. Fortin, M., Vitet, C., Souty-Grosset, C. & Richard, F. J. How do familiarity and relatedness influence mate choice in Armadillidium vulgare? PLoS ONE 13, e0209893 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Tuni, C., Mestre, L., Berger-Tal, R., Lubin, Y. & Bilde, T. Mate choice in naturally inbred spiders: testing the role of relatedness. Anim. Behav. 157, 27–33 (2019).

    Article  Google Scholar 

  63. Ruch, J., Heinrich, L., Bilde, T. & Schneider, J. M. The evolution of social inbreeding mating systems in spiders: limited male mating dispersal and lack of pre-copulatory inbreeding avoidance in a subsocial predecessor. Biol. J. Linn. Soc. 98, 851–859 (2009).

    Article  Google Scholar 

  64. Bilde, T., Lubin, Y., Smith, D., Schneider, J. M. & Maklakov, A. A. The transition to social inbred mating systems in spiders: role of inbreeding tolerance in a subsocial predecessor. Evolution 59, 160–174 (2005).

    PubMed  Google Scholar 

  65. Welke, K. W. & Schneider, J. M. Males of the orb-web spider Argiope bruennichi sacrifice themselves to unrelated females. Biol. Lett. 6, 585–588 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Welke, K. & Schneider, J. M. Inbreeding avoidance through cryptic female choice in the cannibalistic orb-web spider Argiope lobata. Behav. Ecol. 20, 1056–1062 (2009).

    Article  Google Scholar 

  67. Chen, Z. et al. Inbreeding produces trade-offs between maternal fecundity and offspring survival in a monandrous spider. Anim. Behav. 132, 253–259 (2017).

    Article  Google Scholar 

  68. Zeh, J. A. & Zeh, D. W. Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females. Nature 439, 201–203 (2006).

    Article  CAS  PubMed  Google Scholar 

  69. McCarthy, T. M. & Sih, A. Relatedness of mates influences mating behaviour and reproductive success of the hermaphroditic freshwater snail Physa gyrina. Evol. Ecol. Res. 10, 77–94 (2008).

    Google Scholar 

  70. Facon, B., Ravigné, V. & Goudet, J. Experimental evidence of inbreeding avoidance in the hermaphroditic snail Physa acuta. Evol. Ecol. 20, 395–406 (2006).

    Article  Google Scholar 

  71. Baur, B. & Baur, A. Random mating with respect to relatedness in the simultaneously hermaphroditic land snail Arianta arbustorum. Invertebr. Biol. 116, 294–298 (1997).

    Article  Google Scholar 

  72. Ng, T. P. T. & Johannesson, K. No precopulatory inbreeding avoidance in the intertidal snail Littorina saxatilis. J. Mollusca. Stud. 82, 213–215 (2015).

    Google Scholar 

  73. Burgess, S. C., Sander, L. & Bueno, M. How relatedness between mates influences reproductive success: an experimental analysis of self-fertilization and biparental inbreeding in a marine bryozoan. Ecol. Evol. 9, 11353–11366 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Peters, A. & Michiels, N. K. Evidence for lack of inbreeding avoidance by selective mating in a simultaneous hermaphrodite. Invertebr. Biol. 115, 99–103 (1996).

    Article  Google Scholar 

  75. Boyd, S. K. & Blaustein, A. R. Familiarity and inbreeding avoidance in the gray-tailed vole (Microtus canicaudus). J. Mammal. 66, 348–352 (1985).

    Article  Google Scholar 

  76. Bollinger, E. K., Harper, S. J., Kramer, J. M. & Barrett, G. W. Avoidance of inbreeding in the meadow vole (Microtus pennsylvanicus). J. Mammal. 72, 419–421 (1991).

    Article  Google Scholar 

  77. Sun, P., Zhu, W. & Zhao, X. Opposite-sex sibling recognition in adult root vole, Microtus Oeconomus pallas: phenotype matching or association. Pol. J. Ecol. 56, 701–708 (2008).

    Google Scholar 

  78. Fadao, T., Ruyong, S. & Tingzheng, W. Does low fecundity reflect kin recognition and inbreeding avoidance in the mandarin vole (Microtus mandarinus)? Can. J. Zool. 80, 2150–2155 (2002).

    Article  Google Scholar 

  79. Fadao, T., Tingzheng, W. & Yajun, Z. Inbreeding avoidance and mate choice in the mandarin vole (Microtus mandarinus). Can. J. Zool. 78, 2119–2125 (2000).

    Article  Google Scholar 

  80. Yu, X., Sun, R. & Fang, J. Effect of kinship on social behaviors in Brandt’s voles (Microtus brandti). J. Ethol. 22, 17–22 (2004).

    Article  Google Scholar 

  81. Lucia, K. E. & Keane, B. A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles. Behav. Ecol. Sociobiol. 66, 13–27 (2011).

    Article  Google Scholar 

  82. Gavish, L., Hofmann, J. E. & Getz, L. L. Sibling recognition in the prairie vole, Microtus ochrogaster. Anim. Behav. 32, 362–366 (1984).

    Article  Google Scholar 

  83. Ylӧnen, H. & Haapakoski, M. Risk of inbreeding: problem of mate choice and fitness effects? Isr. J. Ecol. Evol. 62, 155–161 (2016).

    Article  Google Scholar 

  84. Kruczek, M. & Golas, A. Behavioural development of conspecific odour preferences in bank voles, Clethrionomys glareolus. Behav. Process. 64, 31–39 (2003).

    Article  Google Scholar 

  85. Lemaître, J.-F., Ramm, S. A., Hurst, J. L. & Stockley, P. Inbreeding avoidance behaviour of male bank voles in relation to social status. Anim. Behav. 83, 453–457 (2012).

    Article  Google Scholar 

  86. Kruczek, M. Recognition of kin in bank voles (Clethrionomys glareolus). Physiol. Behav. 90, 483–489 (2007).

    Article  CAS  PubMed  Google Scholar 

  87. Rao, X., Zhang, J.-X., Liu, D. & Cong, L. Kinship alters the effects of forced cohabitation on body weight, mate choice and fitness in the rat-like hamster Tscheskia triton. Curr. Zool. 55, 41–47 (2009).

    Article  Google Scholar 

  88. Mateo, J. M. & Johnston, R. E. Kin recognition and the ‘armpit effect’: evidence of self-referent phenotype matching. Proc. Biol. Sci. 267, 695–700 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Grau, H. J. Kin recognition in white-footed deermice (Peromyscus leucopus). Anim. Behav. 30, 497–505 (1982).

    Article  Google Scholar 

  90. Pillay, N. Father–daughter recognition and inbreeding avoidance in the striped mouse, Rhabdomys pumilio. Mamm. Biol. 67, 212–218 (2002).

    Article  Google Scholar 

  91. Pillay, N. & Rymer, T. L. Preference for outbreeding in inbred Littledale’s whistling rats Parotomys littledalei. Evol. Biol. 44, 21–30 (2016).

    Article  Google Scholar 

  92. Pillay, N. Inbreeding in Littledale’s whistling rat Parotomys littledalei. J. Exp. Zool. 293, 171–178 (2002).

    Article  PubMed  Google Scholar 

  93. Firman, R. C. & Simmons, L. W. Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62, 603–611 (2008).

    Article  PubMed  Google Scholar 

  94. Firman, R. C. & Simmons, L. W. Gametic interactions promote inbreeding avoidance in house mice. Ecol. Lett. 18, 937–943 (2015).

    Article  PubMed  Google Scholar 

  95. Barnard, C. J. & Fitzsimons, J. Kin recognition and mate choice in mice: the effects of kinship, familiarity and social interference on intersexual interaction. Anim. Behav. 36, 1078–1090 (1988).

    Article  Google Scholar 

  96. Krackow, S. & Matuschak, B. Mate choice for non-siblings in wild house mice: evidence from a choice test and a reproductive test. Ethology 88, 99–108 (2010).

    Article  Google Scholar 

  97. Musolf, K., Hoffmann, F. & Penn, D. J. Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Anim. Behav. 79, 757–764 (2010).

    Article  Google Scholar 

  98. Bolton, J. L. et al. Kin discrimination in prepubescent and adult Long-Evans rats. Behav. Process. 90, 415–419 (2012).

    Article  Google Scholar 

  99. Valsecchi, P., Razzoli, M. & Choleris, E. Influence of kinship and familiarity on the social and reproductive behaviour of female Mongolian gerbils. Ethol. Ecol. Evol. 14, 239–253 (2002).

    Article  Google Scholar 

  100. Smith, B. A. & Block, M. L. Male saliva cues and female social choice in Mongolian gerbils. Physiol. Behav. 50, 379–384 (1991).

    Article  CAS  PubMed  Google Scholar 

  101. Ågren, G. Two laboratory experiments on inbreeding avoidance in the Mongolian gerbil. Behav. Process. 6, 291–297 (1981).

    Article  Google Scholar 

  102. Ågren, G. Incest avoidance and bonding between siblings in gerbils. Behav. Ecol. Sociobiol. 14, 161–169 (1984).

    Article  Google Scholar 

  103. Ågren, G. Alternative mating strategies in the Mongolian gerbil. Behaviour 91, 229–243 (1984).

    Article  Google Scholar 

  104. Heth, G., Todrank, J., Begall, S., Wegner, R. E. & Burda, H. Genetic relatedness discrimination in eusocial Cryptomys anselli mole-rats, Bathyergidae, Rodentia. Folia Zool. 53, 269–278 (2004).

    Google Scholar 

  105. Bennett, N. C., Faulkes, C. G. & Molteno, A. J. Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility. Proc. Biol. Sci. 263, 1599–1603 (1996).

    Article  CAS  PubMed  Google Scholar 

  106. Carter, S. N., Goldman, B. D., Goldman, S. L. & Freeman, D. A. Social cues elicit sexual behavior in subordinate Damaraland mole-rats independent of gonadal status. Horm. Behav. 65, 14–21 (2014).

    Article  PubMed  Google Scholar 

  107. Greeff, J. M. & Bennett, N. C. Causes and consequences of incest avoidance in the cooperatively breeding mole-rat, Cryptomys darlingi (Bathyergidae). Ecol. Lett. 3, 318–328 (2000).

    Article  Google Scholar 

  108. Clarke, F. M. & Faulkes, C. G. Kin discrimination and female mate choice in the naked mole-rat Heterocephalus glaber. Proc. Biol. Sci. 266, 1995–2002 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Marcinkowska, U. M., Moore, F. R. & Rantala, M. J. An experimental test of the Westermarck effect: sex differences in inbreeding avoidance. Behav. Ecol. 24, 842–845 (2013).

    Article  Google Scholar 

  110. Lass-Hennemann, J. et al. Effects of stress on human mating preferences: stressed individuals prefer dissimilar mates. Proc. Biol. Sci. 277, 2175–2183 (2010).

    PubMed  PubMed Central  Google Scholar 

  111. Lass-Hennemann, J. et al. Effect of facial self-resemblance on the startle response and subjective ratings of erotic stimuli in heterosexual men. Arch. Sex. Behav. 40, 1007–1014 (2011).

    Article  PubMed  Google Scholar 

  112. Krupp, D. B., DeBruine, L. M., Jones, B. C. & Lalumiere, M. L. Kin recognition: evidence that humans can perceive both positive and negative relatedness. J. Evol. Biol. 25, 1472–1478 (2012).

    Article  CAS  PubMed  Google Scholar 

  113. Kocsor, F., Rezneki, R., Juhasz, S. & Bereczkei, T. Preference for facial self-resemblance and attractiveness in human mate choice. Arch. Sex. Behav. 40, 1263–1270 (2011).

    Article  PubMed  Google Scholar 

  114. Finke, J. B., Zhang, X., Best, D. R., Lass-Hennemann, J. & Schächinger, H. Self-resemblance modulates processing of socio-emotional pictures in a context-sensitive manner. J. Psychophysiol. 33, 127–138 (2019).

    Article  Google Scholar 

  115. Fraley, R. C. & Marks, M. J. Westermarck, Freud, and the incest taboo: does familial resemblance activate sexual attraction? Pers. Soc. Psychol. Bull. 36, 1202–1212 (2010).

    Article  PubMed  Google Scholar 

  116. Henkel, S. & Setchell, J. M. Group and kin recognition via olfactory cues in chimpanzees (Pan troglodytes). Proc. Biol. Sci. 285, https://doi.org/10.1098/rspb.2018.1527 (2018)

  117. Pfefferle, D., Kazem, A. J., Brockhausen, R. R., Ruiz-Lambides, A. V. & Widdig, A. Monkeys spontaneously discriminate their unfamiliar paternal kin under natural conditions using facial cues. Curr. Biol. 24, 1806–1810 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Pfefferle, D., Ruiz-Lambides, A. V. & Widdig, A. Male rhesus macaques use vocalizations to distinguish female maternal, but not paternal, kin from non-kin. Behav. Ecol. Sociobiol. 69, 1677–1686 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Erhart, E. M., Coelho, A. M. Jr. & Bramblett, C. A. Kin recognition by paternal half-siblings in captive Papio cynocephalus. Am. J. Primatol. 43, 147–157 (1997).

    Article  CAS  PubMed  Google Scholar 

  120. Craul, M., Zimmermann, E. & Radespiel, U. First experimental evidence for female mate choice in a nocturnal primate. Primates 45, 271–274 (2004).

    Article  PubMed  Google Scholar 

  121. Mossotti, R. H. et al. Reactions of female cheetahs (Acinonyx jubatus) to urine volatiles from males of varying genetic distance. Zoo Biol. 37, 229–235 (2018).

    Article  Google Scholar 

  122. Hamilton, J. & Vonk, J. Do dogs (Canis lupus familiaris) prefer family? Behav. Process. 119, 123–134 (2015).

    Article  Google Scholar 

  123. Orihuela, A. & Vázquez, R. Mating preferences of Saint Croix rams to related or unrelated ewes. Small Rumin. Res. 83, 82–84 (2009).

    Article  Google Scholar 

  124. Fracasso, G., Tuliozi, B., Hoi, H. & Griggio, M. Can house sparrows recognize familiar or kin-related individuals by scent? Curr. Zool. 65, 53–59 (2019).

    Article  PubMed  Google Scholar 

  125. Schielzeth, H., Burger, C., Bolund, E. & Forstmeier, W. Assortative versus disassortative mating preferences of female zebra finches based on self-referent phenotype matching. Anim. Behav. 76, 1927–1934 (2008).

    Article  Google Scholar 

  126. Miller, D. B. Long-term recognition of father’s song by female zebra finches. Nature 280, 389–391 (1979).

    Article  Google Scholar 

  127. Burley, N., Minor, C. & Strachan, C. Social preference of zebra finches for siblings, cousins and non-kin. Anim. Behav. 39, 775–784 (1990).

    Article  Google Scholar 

  128. Kato, Y., Hasegawa, T. & Okanoya, K. Song preference of female Bengalese finches as measured by operant conditioning. J. Ethol. 28, 447–453 (2010).

    Article  Google Scholar 

  129. Schubert, C. A., Ratcliffe, L. M. & Boag, P. T. A test of inbreeding avoidance in the zebra finch. Ethology 82, 265–274 (2010).

    Article  Google Scholar 

  130. Slater, P. J. B. & Clements, F. A. Incestuous mating in zebra finches. Z. Tierpsychol. 57, 201–208 (2010).

    Article  Google Scholar 

  131. Arct, A., Rutkowska, J., Martyka, R., Drobniak, S. M. & Cichon, M. Kin recognition and adjustment of reproductive effort in zebra finches. Biol. Lett. 6, 762–764 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Bonadonna, F. & Sanz-Aguilar, A. Kin recognition and inbreeding avoidance in wild birds: the first evidence for individual kin-related odour recognition. Anim. Behav. 84, 509–513 (2012).

    Article  Google Scholar 

  133. Vuarin, P. et al. No evidence for prezygotic postcopulatory avoidance of kin despite high inbreeding depression. Mol. Ecol. 27, 5252–5262 (2018).

    Article  PubMed  Google Scholar 

  134. Bateson, P. Preferences for cousins in Japanese quail. Nature 295, 236–237 (1982).

    Article  Google Scholar 

  135. Løvlie, H., Gillingham, M. A., Worley, K., Pizzari, T. & Richardson, D. S. Cryptic female choice favours sperm from major histocompatibility complex-dissimilar males. Proc. Biol. Sci. 280, 20131296 (2013).

    PubMed  PubMed Central  Google Scholar 

  136. Pizzari, T., Lovlie, H. & Cornwallis, C. K. Sex-specific, counteracting responses to inbreeding in a bird. Proc. Biol. Sci. 271, 2115–2121 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  137. Denk, A. G., Holzmann, A., Peters, A., Vermeirssen, E. L. M. & Kempenaers, B. Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav. Ecol. 16, 825–833 (2005).

    Article  Google Scholar 

  138. Jansson, N., Uller, T. & Olsson, M. Female dragons, Ctenophorus pictus, do not prefer scent from unrelated males. Aust. J. Zool. 53, 279–282 (2005).

    Article  Google Scholar 

  139. Ala-Honkola, O., Tuominen, L. & Lindström, K. Inbreeding avoidance in a poeciliid fish (Heterandria formosa). Behav. Ecol. Sociobiol. 64, 1403–1414 (2010).

    Article  Google Scholar 

  140. Vega-Trejo, R., Head, M. L. & Jennions, M. D. Evidence for inbreeding depression in a species with limited opportunity for maternal effects. Ecol. Evol. 5, 1398–1404 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  141. Pitcher, T. E., Rodd, F. H. & Rowe, L. Female choice and the relatedness of mates in the guppy (Poecilia reticulata): mate choice and inbreeding depression. Genetica 134, 137–146 (2008).

    Article  PubMed  Google Scholar 

  142. Daniel, M. J. & Rodd, F. H. Female guppies can recognize kin but only avoid incest when previously mated. Behav. Ecol. 27, 55–61 (2016).

    Article  Google Scholar 

  143. Fitzpatrick, L. J., Gasparini, C., Fitzpatrick, J. L. & Evans, J. P. Male–female relatedness and patterns of male reproductive investment in guppies. Biol. Lett. 10, 20140166 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  144. Viken, A., Fleming, I. A. & Rosenqvist, G. Premating avoidance of inbreeding absent in female guppies (Poecilia reticulata). Ethology 112, 716–723 (2006).

    Article  Google Scholar 

  145. Gasparini, C. & Pilastro, A. Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. Biol. Sci. 278, 2495–2501 (2011).

    PubMed  PubMed Central  Google Scholar 

  146. Evans, J. P., Brooks, R. C., Zajitschek, S. R. & Griffith, S. C. Does genetic relatedness of mates influence competitive fertilization success in guppies? Evolution 62, 2929–2935 (2008).

    Article  PubMed  Google Scholar 

  147. Fitzpatrick, J. L. & Evans, J. P. Postcopulatory inbreeding avoidance in guppies. J. Evol. Biol. 27, 2585–2594 (2014).

    Article  CAS  PubMed  Google Scholar 

  148. Speechley, E. M., Gasparini, C. & Evans, J. P. Female guppies increase their propensity for polyandry as an inbreeding avoidance strategy. Anim. Behav. 157, 87–93 (2019).

    Article  Google Scholar 

  149. Thünken, T., Bakker, T. C. M., Baldauf, S. A. & Kullmann, H. Active inbreeding in a cichlid fish and its adaptive significance. Curr. Biol. 17, 225–229 (2007).

    Article  PubMed  Google Scholar 

  150. Thünken, T., Bakker, T. C. M., Baldauf, S. A. & Kullmann, H. Direct familiarity does not alter mating preference for sisters in male Pelvicachromis taeniatus (Cichlidae). Ethology 113, 1107–1112 (2007).

    Article  Google Scholar 

  151. Thünken, T., Meuthen, D., Bakker, T. C. M. & Baldauf, S. A. A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice. Proc. Biol. Sci. 279, 2959–2964 (2012).

    PubMed  PubMed Central  Google Scholar 

  152. Thünken, T., Bakker, T. C. M. & Baldauf, S. A. ‘Armpit effect’ in an African cichlid fish: self-referent kin recognition in mating decisions of male Pelvicachromis taeniatus. Behav. Ecol. Sociobiol. 68, 99–104 (2013).

    Article  Google Scholar 

  153. Frommen, J. G. & Bakker, T. C. Inbreeding avoidance through non-random mating in sticklebacks. Biol. Lett. 2, 232–235 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  154. Butts, I. A., Johnson, K., Wilson, C. C. & Pitcher, T. E. Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush. Theriogenology 78, 2105–2109 e2101 (2012).

    Article  CAS  PubMed  Google Scholar 

  155. Gerlach, G. & Lysiak, N. Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim. Behav. 71, 1371–1377 (2006).

    Article  Google Scholar 

  156. Kueffer, C. et al. Fame, glory and neglect in meta-analyses. Trends Ecol. Evol. 26, 493–494 (2011).

    Article  PubMed  Google Scholar 

  157. Cohen, J. Statistical Power Analysis for the Behavioral Sciences, 2nd edn (Lawrence Erlbaum, 1988).

  158. Blouin, M. S. DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol. Evol. 18, 503–511 (2003).

    Article  Google Scholar 

  159. Brown, J. L. & Eklund, A. Kin recognition and the major histocompatibility complex: an integrative review. Am. Nat. 143, 435–461 (1994).

    Article  Google Scholar 

  160. Penn, D. J. The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108, 1–21 (2002).

    Article  Google Scholar 

  161. Kokko, H. & Mappes, J. Sexual selection when fertilization is not guaranteed. Evolution 59, 1876–1885 (2005).

    PubMed  Google Scholar 

  162. Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R. & Rushton, L. Performance of the trim and fill method in the presence of publication bias and between-study heterogeneity. Stat. Med. 26, 4544–4562 (2007).

    Article  PubMed  Google Scholar 

  163. Nakagawa, S. & Santos, E. S. A. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 26, 1253–1274 (2012).

    Article  Google Scholar 

  164. Senior, A. M. et al. Heterogeneity in ecological and evolutionary meta-analyses: its magnitude and implications. Ecology 97, 3293–3299 (2016).

    Article  PubMed  Google Scholar 

  165. Zeh, J. A. & Zeh, D. W. The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc. R. Soc. B 264, 69–75 (1997).

    Article  PubMed Central  Google Scholar 

  166. Carleial, R. et al. Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition. Philos. Trans. R. Soc. Lond. B 375, 20200081 (2020).

    Article  Google Scholar 

  167. Antfolk, J. et al. Opposition to inbreeding between close kin reflects inclusive fitness costs. Front. Psychol. 9, 2101 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  168. Kresanov, P. et al. Intergenerational incest aversion: self-reported sexual arousal and disgust to hypothetical sexual contact with family members. Evol. Hum. Behav. 39, 664–674 (2018).

    Article  Google Scholar 

  169. Richardson, J., Comin, P. & Smiseth, P. T. Inbred burying beetles suffer fitness costs from making poor decisions. Proc. R. Soc. B 285, 20180419 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  170. Long, T. A. F., Rowe, L. & Agrawal, A. F. The effects of selective history and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster. Am. Nat. 181, 532–544 (2013).

    Article  PubMed  Google Scholar 

  171. Johnson, A. M. et al. Inbreeding depression and inbreeding avoidance in a natural population of guppies (Poecilia reticulata). Ethology 116, 448–457 (2010).

    Article  Google Scholar 

  172. Barson, N., Cable, J. & Van Oosterhout, C. Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source–sink metapopulation structure, founder events and population bottlenecks. J. Evol. Biol. 22, 485–497 (2009).

    Article  CAS  PubMed  Google Scholar 

  173. Lindholm, A. K. et al. Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol. Ecol. 14, 3671–3682 (2005).

    Article  CAS  PubMed  Google Scholar 

  174. Hosken, D. J. & Blanckenhorn, W. U. Female multiple mating, inbreeding avoidance, and fitness: it is not only the magnitude of costs and benefits that counts. Behav. Ecol. 10, 462–464 (1999).

    Article  Google Scholar 

  175. Duthie, A. B. & Reid, J. M. What happens after inbreeding avoidance? Inbreeding by rejected relatives and the inclusive fitness benefit of inbreeding avoidance. PLoS ONE 10, e0125140 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  176. Taylor, H. R. The use and abuse of genetic marker-based estimates of relatedness and inbreeding. Ecol. Evol. 5, 3140–3150 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  177. Galla, S. J. et al. A comparison of pedigree, genetic and genomic estimates of relatedness for informing pairing decisions in two critically endangered birds: implications for conservation breeding programmes worldwide. Evol. Appl. 13, 991–1008 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  178. Charlesworth, B. & Hughes, K. A. Age-specific inbreeding depression and components of genetic variance in relation to the evolution of senescence. Proc. Natl Acad. Sci. USA. 93, 6140 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Janicke, T., Vellnow, N., Sarda, V. & David, P. Sex-specific inbreeding depression depends on the strength of male–male competition. Evolution 67, 2861–2875 (2013).

    PubMed  Google Scholar 

  180. Armbruster, P. & Reed, D. H. Inbreeding depression in benign and stressful environments. Heredity (Edinb.) 95, 235–242 (2005).

    Article  CAS  Google Scholar 

  181. Lüpold, S., de Boer, R. A., Evans, J. P., Tomkins, J. L. & Fitzpatrick, J. L. How sperm competition shapes the evolution of testes and sperm: a meta-analysis. Philos. Trans. R. Soc. Lond. B 375, 20200064 (2020).

    Article  Google Scholar 

  182. Martin-Wintle, M. S. et al. Free mate choice enhances conservation breeding in the endangered giant panda. Nat. Commun. 6, 10125 (2015).

    Article  CAS  PubMed  Google Scholar 

  183. Martin-Wintle, M. S., Wintle, N. J. P., Díez-León, M., Swaisgood, R. R. & Asa, C. S. Improving the sustainability of ex situ populations with mate choice. Zoo Biol. 38, 119–132 (2019).

    Article  PubMed  Google Scholar 

  184. Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G. & Group, P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6, e1000097 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  185. Ouzzani, M., Hammady, H., Fedorowicz, Z. & Elmagarmid, A. Rayyan–a web and mobile app for systematic reviews. Syst. Rev. 5, 210 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  186. Pick, J. L., Nakagawa, S., Noble, D. W. A. & Price, S. Reproducible, flexible and high-throughput data extraction from primary literature: the metaDigitise R package. Methods Ecol. Evol. 10, 426–431 (2019).

    Article  Google Scholar 

  187. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2012).

  188. Hedges, L. & Olkin, I. Statistical Methods for Meta-analysis (Academic, 1985).

  189. Rosenberg, M. S., Rothstein, H. R. & Gurevitch, J. in Handbook of Meta-analysis in Ecology and Evolution (eds Koricheva, J. et al.) 61–71 (Princeton Univ. Press, 2013).

  190. Viechtbauer, W. Conducting meta‐analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

    Article  Google Scholar 

  191. Del Re, A. compute.es: compute effect sizes, R package version 0.2-2 (2013).

  192. Michonneau, F., Brown, J. W., Winter, D. J. & Fitzjohn, R. rotl: an R package to interact with the Open Tree of Life data. Methods Ecol. Evol. 7, 1476–1481 (2016).

    Article  Google Scholar 

  193. Nakagawa, S. & Schielzeth, H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 85, 935–956 (2010).

    PubMed  Google Scholar 

  194. Higgins, J. & Green, S. Cochrane Handbook for Systematic Reviews of Interventions (Wiley-Blackwell, 2009).

  195. Kossmeier, M., Tran, U. S. & Voracek, M. metaviz: forest plots, funnel plots, and visual funnel plot inference for meta-analysis, R package version 0.3.0 https://CRAN.R-project.org/package=metaviz (2018).

  196. Peters, J. L., Sutton, A. J., Jones, D. R., Abrams, K. R. & Rushton, L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J. Clin. Epidemiol. 61, 991–996 (2008).

    Article  PubMed  Google Scholar 

  197. Egger, M., Davey Smith, G., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 315, 629–634 (1997).

    Article  CAS  Google Scholar 

  198. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  199. Duval, S. & Tweedie, R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56, 455–463 (2000).

    Article  CAS  PubMed  Google Scholar 

  200. Shi, L. & Lin, L. The trim-and-fill method for publication bias: practical guidelines and recommendations based on a large database of meta-analyses. Med. (Baltim.) 98, e15987 (2019).

    Article  Google Scholar 

  201. Duval, S. & Tweedie, R. A nonparametric ‘trim and fill’ method of accounting for publication bias in meta-analysis. J. Am. Stat. Assoc. 95, 89–98 (2000).

    Google Scholar 

  202. Møller, A. & Jennions, M. D. How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132, 492–500 (2002).

    Article  PubMed  Google Scholar 

  203. Szulkin, M. & Sheldon, B. C. The environmental dependence of inbreeding depression in a wild bird population. PLoS ONE 2, e1027 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  204. Zeh, D. W. & Zeh, J. A. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. Bioessays 22, 938–946 (2000).

    Article  CAS  PubMed  Google Scholar 

  205. Waser, P. M., Austad, S. N. & Keane, B. When should animals tolerate inbreeding? Am. Nat. 128, 529–537 (1986).

    Article  Google Scholar 

  206. Puurtinen, M. Mate choice for optimal (k)inbreeding. Evolution 65, 1501–1505 (2011).

    Article  PubMed  Google Scholar 

  207. Tregenza, T. & Wedell, N. Polyandrous females avoid costs of inbreeding. Nature 415, 71–73 (2002).

    Article  CAS  PubMed  Google Scholar 

  208. Birkhead, T. R. & Pizzari, T. Postcopulatory sexual selection. Nat. Rev. Genet. 3, 262–273 (2002).

    Article  CAS  PubMed  Google Scholar 

  209. Duthie, A. B., Bocedi, G., Germain, R. R. & Reid, J. M. Evolution of precopulatory and post-copulatory strategies of inbreeding avoidance and associated polyandry. J. Evol. Biol. 31, 31–45 (2018).

    Article  CAS  PubMed  Google Scholar 

  210. Barry, K. L. & Kokko, H. Male mate choice: why sequential choice can make its evolution difficult. Anim. Behav. 80, 163–169 (2010).

    Article  Google Scholar 

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Acknowledgements

We thank S. Nakagawa for his valuable and excellent course on meta-analyses, R. O’Dea for her help with coding and statistical advice and A. Silva for helping create the phylogenetic figure. R.A.d.B. was funded by the Carl Tryggers Foundation (17:152), R.V.-T. and A.K. by the Swedish Research Council (2017-04957) and J.L.F. by the Knut and Alice Wallenberg Foundation and the Swedish Research Council (2017–04680).

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  1. These authors contributed equally: Raïssa A. de Boer, Regina Vega-Trejo.

Authors and Affiliations

  1. Department of Zoology: Ethology, Stockholm University, Stockholm, Sweden

    Raïssa A. de Boer, Regina Vega-Trejo, Alexander Kotrschal & John L. Fitzpatrick

  2. Department of Animal Sciences: Behavioural Ecology, Wageningen University & Research, Wageningen, the Netherlands

    Alexander Kotrschal

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All authors conceived the study and contributed to the design of the study. R.A.d.B. and R.V.-T. collected the data, performed the analyses and wrote the first draft. J.L.F. contributed to interpreting the data and writing the final manuscript. A.K. helped improve the final manuscript.

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Extended data

Extended Data Fig. 1 Phylogenetic distribution of the species included in the dataset.

Primary study references and graphical summary of the phylogenetic distribution of (a) invertebrate and (b) vertebrate species contributing statistical effects addressing inbreeding avoidance. Depicted are phylogenetic relatedness, scientific names, number of effect sizes for precopulatory, during mating, and postcopulatory estimates, and number of studies for each species. Larger numbers of effect sizes are highlighted with darker colouration. Animal silhouettes obtained from phylopic.org.

Extended Data Fig. 2 Assessing publication bias.

The results of Egger’s regressions and adjusted estimates obtained using trim-and-fill methods when assessing the (a) full dataset and (b-d) different subsets of the full dataset. The full dataset was subsetted (as described in the main text and Table 1 legend) to focus only on (b) internal fertilizers, (c) internal fertilizers where kin at relatedness levels of r = 0.5 were assessed, and (d) internal fertilizers where kin at relatedness levels of r = 0.5 were assessed and where kin were familiar and non-kin unfamiliar. For each Egger’s regression model, the intercept, t-value (t), and P-value (P) are provided. Positive intercepts in Egger’s regressions that are significantly different from zero indicate publication bias towards studies confirming kin avoidance. Publication bias in favour of studies reporting kin avoidance was evident in the full dataset and every subset of the dataset examined. In addition, the adjusted estimate (Hedges’ g) and it’s 95% confidence interval [95% CI] for each meta-analytic model is presented, after assessing publication bias using three different estimators (L0, R0 and Q0) to apply the trim-and-fill method.

Extended Data Fig. 3

PRISMA diagram describing the search results in Scopus and Web of Science and the different steps of selecting articles for inclusion in the meta-analysis. In Search A – D different sets of keywords were used to target a wide range of animal studies, and Search E specifically targeted studies on inbreeding avoidance in humans. A backward search was performed on the 10 most recent papers selected for inclusion, and a forward search on the 10 most cited papers selected for inclusion. Details of each search are provided at https://osf.io/e34s9/.

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de Boer, R.A., Vega-Trejo, R., Kotrschal, A. et al. Meta-analytic evidence that animals rarely avoid inbreeding. Nat Ecol Evol 5, 949–964 (2021). https://doi.org/10.1038/s41559-021-01453-9

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