Is Inbreeding the Norm in Nature?

0
10

References

  1. 1.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  2. 2.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  3. 3.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  4. 4.

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

    Article 

    Google Scholar
     

  5. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  6. 6.

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

  7. 7.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  8. 8.

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

  9. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  10. 10.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  11. 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. 12.

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

    CAS 
    Article 

    Google Scholar
     

  13. 13.

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

    Article 

    Google Scholar
     

  14. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  15. 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. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  17. 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. 18.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  19. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  21. 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 
    Article 
    PubMed Central 

    Google Scholar
     

  22. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  23. 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. 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. 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. 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. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  28. 28.

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

    Article 

    Google Scholar
     

  29. 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. 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. 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. 32.

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

    Article 

    Google Scholar
     

  33. 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. 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. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  36. 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. 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. 38.

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

    Article 

    Google Scholar
     

  39. 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. 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. 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. 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).

    PubMed 
    PubMed Central 

    Google Scholar
     

  43. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  45. 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. 46.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  47. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  48. 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. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  50. 50.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  51. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  52. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  53. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  54. 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).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  55. 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. 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. 57.

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

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  58. 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. 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. 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. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  62. 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. 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. 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 
    Article 
    PubMed Central 

    Google Scholar
     

  65. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  66. 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. 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. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  69. 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. 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. 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. 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. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  74. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 86.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  87. 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. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  89. 89.

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

    Article 

    Google Scholar
     

  90. 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. 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. 92.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  93. 93.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  94. 94.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  95. 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. 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. 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. 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. 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. 100.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  101. 101.

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

    Article 

    Google Scholar
     

  102. 102.

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

    Article 

    Google Scholar
     

  103. 103.

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

    Article 

    Google Scholar
     

  104. 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. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  106. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  107. 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. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  109. 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. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  112. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  113. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  114. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  116. 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. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  118. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  119. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  120. 120.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  121. 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. 122.

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

    Article 

    Google Scholar
     

  123. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  125. 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. 126.

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

    Article 

    Google Scholar
     

  127. 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. 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. 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. 130.

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

    Article 

    Google Scholar
     

  131. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  132. 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. 133.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  134. 134.

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

    Article 

    Google Scholar
     

  135. 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. 136.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  137. 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. 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. 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. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  141. 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).

    PubMed 
    Article 

    Google Scholar
     

  142. 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. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  144. 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. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  147. 147.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  148. 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. 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).

    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar
     

  150. 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. 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. 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. 153.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  154. 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).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  155. 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. 156.

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

    PubMed 
    Article 

    Google Scholar
     

  157. 157.

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

  158. 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. 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. 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. 161.

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

    PubMed 
    Article 

    Google Scholar
     

  162. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  163. 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. 164.

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

    PubMed 
    Article 

    Google Scholar
     

  165. 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 

    Google Scholar
     

  166. 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. 167.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  168. 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. 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).

    PubMed 
    Article 

    Google Scholar
     

  170. 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).

    PubMed 
    Article 

    Google Scholar
     

  171. 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. 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).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  173. 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).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  174. 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. 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).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  176. 176.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  177. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  178. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  179. 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 
    Article 
    CAS 
    PubMed Central 

    Google Scholar
     

  180. 180.

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

    CAS 
    Article 

    Google Scholar
     

  181. 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. 182.

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

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  183. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  184. 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).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  185. 185.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  186. 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. 187.

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

  188. 188.

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

  189. 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. 190.

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

    Article 

    Google Scholar
     

  191. 191.

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

  192. 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. 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 
    PubMed Central 

    Google Scholar
     

  194. 194.

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

  195. 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. 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).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  197. 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).

    CAS 
    Article 

    Google Scholar
     

  198. 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. 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).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  200. 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. 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. 202.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  203. 203.

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

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  204. 204.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  205. 205.

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

    Article 

    Google Scholar
     

  206. 206.

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

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  207. 207.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  208. 208.

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

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  209. 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).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  210. 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
     

Download references

LEAVE A REPLY

Please enter your comment!
Please enter your name here