Skip to main content
SpringerLink
Log in

Inbreeding and the evolution of sociality in arthropods

  • Review
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Animals have evolved strategies to optimally balance costs and benefits of inbreeding. In social species, these adaptations can have a considerable impact on the structure, the organization, and the functioning of groups. Here, we consider how selection for inbreeding avoidance fashions the social behavior of arthropods, a phylum exhibiting an unparalleled richness of social lifestyles. We first examine life histories and parental investment patterns determining whether individuals should actively avoid or prefer inbreeding. Next, we illustrate the diversity of inbreeding avoidance mechanisms in arthropods, from the dispersal of individuals to the rejection of kin during mate choice and the production of unisexual broods by females. Then, we address the particular case of haplodiploid insects. Finally, we discuss how inbreeding may drive and shape the evolution of arthropods societies along two theoretical pathways.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M et al (2011) Inclusive fitness theory and eusociality. Nature 471:E1–E4

    Article  PubMed  CAS  Google Scholar 

  • Abe Y, Miura K (2002) Does Wolbachia induce unisexuality in oak gall wasps? (Hymenoptera: Cynipidae). Ann Entomol Soc Am 95:583–586

    Article  Google Scholar 

  • Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  PubMed  CAS  Google Scholar 

  • Bateson P (1978) Sexual imprinting and optimal outbreeding. Nature 273:659–660

    Article  PubMed  CAS  Google Scholar 

  • Bateson P (1983) Optimal outbreeding. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 257–277

    Google Scholar 

  • Beekman M, van Stratum P, Veerman A (1999) Selection for non-diapause in the bumblebee Bombus terrestris, with notes on the effect of inbreeding. Entomol Exp Appl 93:69–75

    Article  Google Scholar 

  • Beukeboom LW, Ellers J, van Alphen JJ (2000) Absence of single locus complementary sex determination in the braconid wasps Asobara tabida and Alysia manducator. Heredity 84:29–36

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Blomquist GJ, Bagnères AG (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, UK

    Book  Google Scholar 

  • Blouin SF, Blouin M (1988) Inbreeding avoidance behaviors. Trends Ecol Evol 3:230–233

    Article  PubMed  CAS  Google Scholar 

  • Bourdais D, Hance T (2009) Lack of behavioural evidence for kin avoidance in mate choice in a hymenopteran parasitoid (Hymenoptera: Braconidae). Behav Process 81:92–94

    Article  CAS  Google Scholar 

  • Bourke AFD (2011) Principles of Social Evolution. Oxford University Press, UK

    Google Scholar 

  • Breed MD (1998) Recognition pheromones of the honey bee. Bioscience 48:463–470

    Article  Google Scholar 

  • Bretman A, Wedell N, Tregenza T (2004) Molecular evidence of postcopulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc R Soc B 271:159–164

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bussière LF, Hunt J, Jennions MD, Brooks R (2006) Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus. Evolution 60:792–800

    Article  PubMed  Google Scholar 

  • Cameron EC, Franck P, Oldroyd BP (2004) Genetic structure of nest aggregations and drone congregations of the southeast Asian stingless bee Trigona collina. Mol Ecol 13:2357–2364

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  PubMed  CAS  Google Scholar 

  • Cheptou PO, Donohue K (2011) Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol 189:395–407

    Article  PubMed  Google Scholar 

  • Cornell SJ, Tregenza T (2007) A new theory for the evolution of polyandry as a means of inbreeding avoidance. Proc R Soc B 274:2873–2879

    Article  PubMed  Google Scholar 

  • Costa JT (2006) The other insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • De Luca PA, Cocroft RB (2008) The effects of age and relatedness of mating patterns in thornbug treehoppers: Inbreeding avoidance or inbreeding tolerance? Behav Ecol Sociobiol 62:1869–1875

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Elias J, Mazzi D, Dorn S (2009) No need to discriminate? Reproductive diploid males in a parasitoid with complementary sex determination. PLoS One 4:e6024

    Article  PubMed  CAS  Google Scholar 

  • Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E, Vitalis R, Guillemaud T, Lundgren J, Estoup A (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Curr Biol 21:424–427

    Article  PubMed  CAS  Google Scholar 

  • Fellowes MDE (1998) Do non-social insects get the (kin) recognition they deserve? Ecol Entomol 23:223–227

    Article  Google Scholar 

  • Foster RL (1992) Nestmate recognition as an inbreeding avoidance mechanism in bumble bees (Hymenoptera, Apidae). J Kans Entomol Soc 65:238–243

    Google Scholar 

  • Gamboa GJ, Reeve HK, Ferguson ID, Wacker TL (1986) Nestmate recognition in social wasps: the origin and acquisition of recognition odours. Anim Behav 34:685–695

    Article  Google Scholar 

  • Gerloff CU, Schmid-Hempel P (2005) Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111:67–80

    Article  Google Scholar 

  • Gerloff CU, Ottmer BK, Schmid-Hempel P (2003) Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Funct Ecol 17:582–589

    Article  Google Scholar 

  • Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678–2687

    PubMed  Google Scholar 

  • Goodisman MAD, Crozier RH (2002) Population and colony genetic structure of the primitive termite Mastotermes darwinensis. Evolution 56:70–83

    PubMed  Google Scholar 

  • Goulson D (2010) Bumblebees, their behavior, ecology and conservation. Oxford University Press, New-York

    Google Scholar 

  • Greenberg L (1979) Genetic component of bee odour in kin recognition. Science 206:1095–1097

    Article  PubMed  CAS  Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviours. J Theor Biol 7:1–16

    Article  PubMed  CAS  Google Scholar 

  • Henter HJ (2003) Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa. Evolution 57:1793–1803

    PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. Norton & Co, New-York

    Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216

    Article  PubMed  CAS  Google Scholar 

  • Ivy TM, Weddle CB, Sakaluk SK (2005) Females use self-referent cues to avoid mating with previous mates. Proc R Soc B 272:2475–2478

    Article  PubMed  Google Scholar 

  • Jaffé R, Moritz RFA, Kraus FB (2009) Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii. Popul Ecol 51:227–236

    Article  Google Scholar 

  • Jennions MD, Hunt J, Graham R, Brooks R (2004) No evidence for inbreeding avoidance through postcopulatory mechanisms in the black field cricket, Teleogryllus commodus. Evolution 58:2472–2477

    PubMed  Google Scholar 

  • Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404

    Article  PubMed  CAS  Google Scholar 

  • Keller L, Fournier D (2002) Lack of inbreeding avoidance in the Argentine ant Linepithema humile. Behav Ecol 13:28–31

    Article  Google Scholar 

  • Keller L, Passera L (1993) Incest avoidance, fluctuating asymmetry, and the consequences of inbreeding in Iridomyrmex humilis, an ant with multiple queen colonies. Behav Ecol Sociobiol 33:191–199

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Keller L, Peer K, Bernasconi C, Taborsky M, Shuker D (2011) Inbreeding and selection on sex ratio in the bark beetle Xylosandrus germanus. BMC Evol Biol 11:359

    Article  PubMed  Google Scholar 

  • Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313–339

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V (2010) Research on inbreeding in the ‘omic’ era. Trends Ecol Evol 25:44–52

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lehtonen J, Kokko H (2012) Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes. Phil Trans Roy Soc B 367:211–221

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Liebert AE, Wilson-Rich N, Johnson CE, Starks PT (2010) Sexual interactions and nestmate recognition in invasive populations of Polistes dominulus wasps. Insect Soc 57:457–463

    Article  Google Scholar 

  • Lihoreau M, Rivault C (2009) Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav Ecol 20:46–53

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lihoreau M, Costa JT, Rivault C (2012) The social biology of domiciliary cockroaches: colony structure, kin recognition and collective decisions. Insect Soc. doi:10.1007/s00040-012-0234-x

  • Mack PD, Hammock BA, Promislow DEL (2002) Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt. Evolution 56:1789–1795

    PubMed  Google Scholar 

  • Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364

    Article  PubMed  CAS  Google Scholar 

  • Nilsson T, Fricke C, Arnqvist G (2002) Patterns of divergence in the effects of mating on female reproductive performance in flour beetles. Evolution 56:111–120

    PubMed  Google Scholar 

  • Nur U, Werren JH, Eickbush DG, Burke WD, Eickbush TH (1988) A Selfish B chromosome that enhances its transmission by eliminating the paternal genome. Science 240:512–514

    Article  PubMed  CAS  Google Scholar 

  • Ode PJ, Antolin MF, Strand MR (1995) Brood-mate avoidance in the parasitic wasp Bracon hebetor Say. Anim Behav 49:1239–1248

    Article  Google Scholar 

  • Page RE Jr (1980) The evolution of multiple mating behavior by honey bee queens (Apis mellifera). Genetics 96:263–273

    PubMed  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, New-York, pp 123–166

    Google Scholar 

  • Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos T R Soc B 361:235–259

    Article  CAS  Google Scholar 

  • Paxton RJ (2000) Genetic structure of colonies and male aggregation in the stingless bee Scaptotrigona postica, as revealed by microsatellite analysis. Insect Soc 47:63–69

    Article  Google Scholar 

  • Peer K, Taborsky M (2004) Female ambrosia beetles adjust their offspring sex ratio according to outbreeding opportunities for their sons. J Evol Biol 17:257–264

    Article  PubMed  CAS  Google Scholar 

  • Peer K, Taborsky M (2005) Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sib mating. Evolution 59:317–323

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608

    Article  PubMed  CAS  Google Scholar 

  • Robinson SP, Kennington WJ, Simmons LW (2012) Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster. J Evol Biol 25:716–725

    Article  PubMed  Google Scholar 

  • Schrempf A, Aron S, Heinze J (2006) Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity 97:75–80

    Article  PubMed  CAS  Google Scholar 

  • Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc B 274:67–72

    Article  PubMed  Google Scholar 

  • Shilpa MC, Sen R, Gadagkar R (2010) Nestmateship and body size do not influence mate choice in males and females: a laboratory study of a primitively eusocial wasp Ropalidia marginata. Behav Process 85:42–46

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Smith BH, Ayasse M (1987) Kin-based male mating preferences in two species of halictine bee. Behav Ecol Sociobiol 20:313–318

    Article  Google Scholar 

  • Soroker V, Vienne C, Hefetz A, Nowbahari E (1994) The postpharyngeal gland as a gestalt organ for nestmate recognition in the ant Cataglyphis niger. Naturwissenschaften 81:510–513

    CAS  Google Scholar 

  • Stockley P, Searle JB, Macdonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc B 254:173–179

    Article  PubMed  CAS  Google Scholar 

  • Stouthamer R, van Tilborg M, de Jong JH, Nunney L, Luck RF (2001) Selfish element maintains sex in natural populations of a parasitoid wasp. Proc R Soc B 268:617–622

    Article  PubMed  CAS  Google Scholar 

  • Strassmann JE, Page RE Jr, Robinson GE, Seeley TD (2011) Kin selection and eusociality. Nature 471:E5–E6

    Article  PubMed  CAS  Google Scholar 

  • Stuart JJ, Hatchett JH (1991) Genetics of sex determination in the Hessian fly, Mayetiola destructor. J Hered 82:43–52

    Google Scholar 

  • Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19:1257–1264

    Article  PubMed  CAS  Google Scholar 

  • Tabadkani SM, Khansefid M, Ashouri A (2011) Monogeny, a neglected mechanism of inbreeding avoidance in small populations of gall midges. Entomol Exp Appl 140:77–84

    Article  Google Scholar 

  • Tabadkani SM, Ashouri A, Farhoudi F (2012a) An equal sex ratio followed by differential sex mortality causes overestimation of females in gall midges: no evidence for sex ratio regulation. Naturwissenschaften 99:493–499

    Article  PubMed  CAS  Google Scholar 

  • Tabadkani SM, Ashouri A, Farhoudi F (2012b) Does monogeny enable gall midges to regulate their sex ratio? Eur J Entomol 109:339–343

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Thornhill NW (1993) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago

    Google Scholar 

  • Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge

    Google Scholar 

  • Thurin N, Aron S (2009) Sib-mating in the ant Plagiolepis pygmaea: adaptative inbreeding? J Evol Biol 22:2481–2487

    Article  PubMed  CAS  Google Scholar 

  • Tien NSH, Massourakis G, Sabelis MW, Egas M (2011) Mate choice promotes inbreeding avoidance in the two-spotted spider mite. Exp Appl Acarol 54:119–124

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine-Atherton, Chicago, pp 136–179

    Google Scholar 

  • van Zweden JS, d'Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, UK, pp 222–243

    Chapter  Google Scholar 

  • Waldbauer CP, Sternburg JC (1979) Inbreeding depression and a behavioral mechanism for its avoidance in Hyalophora cecropia. Am Midl Nat 102:204–208

    Article  Google Scholar 

  • Welke KW, Schneider JM (2010) Males of the orb-web spider Argiope bruennichi sacrifice themselves to unrelated females. Biol Lett 6:585–588

    Article  PubMed  Google Scholar 

  • Werren JH, Hatcher MJ, Godfray HCJ (2002) Maternal-offspring conflict leads to the evolution of dominant zygotic sex determination. Heredity 88:102–111

    Article  PubMed  CAS  Google Scholar 

  • Whitehorn PR, Tinsley MC, Goulson D (2009) Kin recognition and inbreeding reluctance in bumblebees. Apidologie 40:627–633

    Article  Google Scholar 

  • Whiting PW (1943) Multiple alleles in complementary sex determination of Habrobracon. Genetics 24:110–111

    Google Scholar 

  • Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. Proc Natl Acad Sci USA 102:13367–13371

    Article  PubMed  CAS  Google Scholar 

  • Winsor GL, Innes DJ (2002) Sexual reproduction in Daphnia pulex (Crustacea: Cladocera): observations on male mating behavior and avoidance of inbreeding. Freshwat Biol 47:441–450

    Article  Google Scholar 

  • Xu J, Wang Q (2009) A polyandrous female moth discriminates against previous mates to gain genetic diversity. Anim Behav 78:1309–1315

    Article  Google Scholar 

  • Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742–10746

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank three anonymous referees for their constructive comments in an earlier version of this manuscript. We are also grateful to V Rahimi-Alangi and F Farhoudi for their precious help with this work. SMT and JN were funded by the University of Tehran. ML was supported by a postdoctoral fellowship from the Australian Research Council.

Author information

Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Tehran, PO Box 4111, Karaj, Iran

    Seyed Mohammad Tabadkani & Jamasb Nozari

  2. School of Biological Sciences and the Charles Perkins Centre, The University of Sydney, Sydney, NSW, Australia

    Mathieu Lihoreau

Authors
  1. Seyed Mohammad Tabadkani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jamasb Nozari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mathieu Lihoreau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seyed Mohammad Tabadkani.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tabadkani, S.M., Nozari, J. & Lihoreau, M. Inbreeding and the evolution of sociality in arthropods. Naturwissenschaften 99, 779–788 (2012). https://doi.org/10.1007/s00114-012-0961-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-012-0961-x

Keywords

Search

Navigation