Inbreeding and the evolution of sociality in arthropods

Naturwissenschaften

Volumn 99, Issue 10, 2012, Pages 779-788

  Tabadkani, Seyed Mohammad ^a   Nozari, Jamasb ^a   Lihoreau, Mathieu ^b  

^a UNIVERSITY OF TEHRAN   (Iran)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Arthropods; Haplodiploidy; Inbreeding avoidance; Social evolution

Indexed keywords

ADAPTATION; ARTHROPOD; BIOLOGICAL PRODUCTION; DISPERSAL; EUSOCIALITY; GROUP SIZE; INBREEDING; INBREEDING AVOIDANCE; LIFE HISTORY TRAIT; MATE CHOICE; PARENTAL INVESTMENT; REPRODUCTIVE COST; SEXUAL SELECTION; SOCIAL ORGANIZATION;

ANIMAL; ARTHROPOD; EVOLUTION; GENETICS; INBREEDING; PHYSIOLOGY; PLOIDY; REVIEW; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR;

ANIMALS; ARTHROPODS; BIOLOGICAL EVOLUTION; INBREEDING; PLOIDIES; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR;

ANIMALIA; ARTHROPODA; HEXAPODA;

EID: 84866737811     PISSN: 00281042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00114-012-0961-x     Document Type: Review

References (104)

1. Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JAC, Andersson M et al (2011) Inclusive fitness theory and eusociality. Nature 471:E1-E4
2. Abe Y, Miura K (2002) Does Wolbachia induce unisexuality in oak gall wasps? (Hymenoptera: Cynipidae). Ann Entomol Soc Am 95:583-586
3. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697-709
4. Bateson P (1978) Sexual imprinting and optimal outbreeding. Nature 273:659-660
5. Bateson P (1983) Optimal outbreeding. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 257-277
6. 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
7. 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
8. 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
9. Blomquist GJ, Bagnères AG (2010) Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, UK
10. Blouin SF, Blouin M (1988) Inbreeding avoidance behaviors. Trends Ecol Evol 3:230-233
11. 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
12. Bourke AFD (2011) Principles of Social Evolution. Oxford University Press, UK
13. Breed MD (1998) Recognition pheromones of the honey bee. Bioscience 48:463-470
14. 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
15. Bretman A, Newcombe D, Tregenza T (2009) Promiscuous females avoid inbreeding by controlling sperm storage. Mol Ecol 18:3340-3345
16. 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
17. 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
18. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783-796
19. Cheptou PO, Donohue K (2011) Environment-dependent inbreeding depression: its ecological and evolutionary significance. New Phytol 189:395-407
20. 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
21. Costa JT (2006) The other insect societies. Harvard University Press, Cambridge
22. 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
23. 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
24. 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
25. 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
26. Fellowes MDE (1998) Do non-social insects get the (kin) recognition they deserve? Ecol Entomol 23:223-227
27. Foster RL (1992) Nestmate recognition as an inbreeding avoidance mechanism in bumble bees (Hymenoptera, Apidae). J Kans Entomol Soc 65:238-243
28. 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
29. Gerloff CU, Schmid-Hempel P (2005) Inbreeding depression and family variation in a social insect, Bombus terrestris (Hymenoptera: Apidae). Oikos 111:67-80
30. 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
31. Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57:2678-2687
32. Goodisman MAD, Crozier RH (2002) Population and colony genetic structure of the primitive termite Mastotermes darwinensis. Evolution 56:70-83
33. Goulson D (2010) Bumblebees, their behavior, ecology and conservation. Oxford University Press, New-York
34. Greenberg L (1979) Genetic component of bee odour in kin recognition. Science 206:1095-1097
35. Hamilton WD (1964) The genetical evolution of social behaviours. J Theor Biol 7:1-16
36. Henter HJ (2003) Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa. Evolution 57:1793-1803
37. Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. Norton & Co, New-York
38. 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
39. 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
40. 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
41. 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
42. Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402-404
43. Keller L, Fournier D (2002) Lack of inbreeding avoidance in the Argentine ant Linepithema humile. Behav Ecol 13:28-31
44. 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
45. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230-241
46. 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
47. Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313-339
48. Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467-475
49. Kristensen TN, Pedersen KS, Vermeulen CJ, Loeschcke V (2010) Research on inbreeding in the 'omic' era. Trends Ecol Evol 25:44-52
50. Lehmann L, Perrin N (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. Am Nat 162:638-652
51. 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
52. Lewis Z, Wedell N (2009) Male moths reduce sperm investment in relatives. Anim Behav 77:1547-1550
53. 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
54. Lihoreau M, Rivault C (2009) Kin recognition via cuticular hydrocarbons shapes cockroach social life. Behav Ecol 20:46-53
55. Lihoreau M, Rivault C (2010) German cockroach males maximize their inclusive fitness by avoiding mating with kin. Anim Behav 80:303-309
56. Lihoreau M, Zimmer C, Rivault C (2007) Kin recognition and incest avoidance in a group-living insect. Behav Ecol 18:880-887
57. Lihoreau M, Zimmer C, Rivault C (2008) Mutual mate choice: when it pays both sexes to avoid inbreeding. PLoS One 3:e3365
58. 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
59. Mack PD, Hammock BA, Promislow DEL (2002) Sperm competitive ability and genetic relatedness in Drosophila melanogaster: similarity breeds contempt. Evolution 56:1789-1795
60. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362-364
61. 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
62. 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
63. Ode PJ, Antolin MF, Strand MR (1995) Brood-mate avoidance in the parasitic wasp Bracon hebetor Say. Anim Behav 49:1239-1248
64. Page RE Jr (1980) The evolution of multiple mating behavior by honey bee queens (Apis mellifera). Genetics 96:263-273
65. 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
66. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Philos T R Soc B 361:235-259
67. 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
68. 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
69. Peer K, Taborsky M (2005) Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sib mating. Evolution 59:317-323
70. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201-206
71. Puurtinen M (2011) Mate choice for optimal (k) inbreeding. Evolution 65:1501-1505
72. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581-608
73. 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
74. Schrempf A, Aron S, Heinze J (2006) Sex determination and inbreeding depression in an ant with regular sib-mating. Heredity 97:75-80
75. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc B 274:67-72
76. 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
77. 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
78. Smith BH, Ayasse M (1987) Kin-based male mating preferences in two species of halictine bee. Behav Ecol Sociobiol 20:313-318
79. 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
80. 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
81. 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
82. Strassmann JE, Page RE Jr, Robinson GE, Seeley TD (2011) Kin selection and eusociality. Nature 471:E5-E6
83. Stuart JJ, Hatchett JH (1991) Genetics of sex determination in the Hessian fly, Mayetiola destructor. J Hered 82:43-52
84. Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19:1257-1264
85. 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
86. 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
87. Tabadkani SM, Ashouri A, Farhoudi F (2012b) Does monogeny enable gall midges to regulate their sex ratio? Eur J Entomol 109:339-343
88. Teng ZQ, Kang L (2007) Egg-hatching benefits gained by polyandrous female locusts are not due to the fertilization advantage of non-sibling males. Evolution 61:470-476
89. Thornhill NW (1993) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago
90. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge
91. Thurin N, Aron S (2009) Sib-mating in the ant Plagiolepis pygmaea: adaptative inbreeding? J Evol Biol 22:2481-2487
92. 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
93. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71-73
94. 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
95. 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
96. Waldbauer CP, Sternburg JC (1979) Inbreeding depression and a behavioral mechanism for its avoidance in Hyalophora cecropia. Am Midl Nat 102:204-208
97. Welke KW, Schneider JM (2010) Males of the orb-web spider Argiope bruennichi sacrifice themselves to unrelated females. Biol Lett 6:585-588
98. Werren JH, Hatcher MJ, Godfray HCJ (2002) Maternal-offspring conflict leads to the evolution of dominant zygotic sex determination. Heredity 88:102-111
99. Whitehorn PR, Tinsley MC, Goulson D (2009) Kin recognition and inbreeding reluctance in bumblebees. Apidologie 40:627-633
100. Whiting PW (1943) Multiple alleles in complementary sex determination of Habrobracon. Genetics 24:110-111
101. Wilson EO, Hölldobler B (2005) Eusociality: origin and consequences. Proc Natl Acad Sci USA 102:13367-13371
102. 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
103. Xu J, Wang Q (2009) A polyandrous female moth discriminates against previous mates to gain genetic diversity. Anim Behav 78:1309-1315
104. Zayed A, Packer L (2005) Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc Natl Acad Sci USA 102:10742-10746