Inbreeding level does not induce female discrimination between sibs and unrelated males in guppies

Behavioral Ecology and Sociobiology

Volumn 64, Issue 10, 2010, Pages 1601-1607

  Guevara Fiore, Palestina ^a   Rosenqvist, Gunilla ^b   Watt, Penelope J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

Author keywords

Female preference; Mate choice; Odour; Olfactory cues; Sexual selection

Indexed keywords

CYPRINID; INBREEDING AVOIDANCE; KIN RECOGNITION; MATE CHOICE; ODOR; OLFACTORY CUE; PREFERENCE BEHAVIOR; REPRODUCTIVE COST; SEXUAL SELECTION; SIBLING;

CYPRINODONTIFORMES; POECILIA RETICULATA;

EID: 77956762719     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-010-0973-5     Document Type: Article

References (92)

1. Aeschlimann PB, Häberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54: 119-126.
2. Ala-Honkola O, Uddström A, Pauli BD, Lindström K (2009) Strong inbreeding depression in male mating behaviour in a poeciliid fish. J Evol Biol 22: 1396-1406.
3. Archard GA, Cuthill IC, Partridge JC, van Oosterhout C (2008) Female guppies (Poecilia reticulata) show no preference for conspecific chemosensory cues in the field or an artificial flow chamber. Behaviour 145: 1329-1346.
4. Arkush KD, Giese AR, Mendonca HL, McBride AM, Marty GD, Hedrick PW (2002) Resistance to three pathogens in the endangered winter-run chinook salmon (Oncorhynchus tshawytscha): effects of inbreeding and major histocompatibility complex genotypes. Can J Fish Aquat Sci 59: 966-975.
5. Becher SA, Magurran AE (2004) Multiple mating and reproductive skew in Trinidadian guppies. Proc R Soc Biol Sci Series B 271: 1009-1014.
6. 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.
7. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24: 127-135.
8. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8: 60-65.
9. Brown C, Laland KN, Krause J (2006) Fish cognition and behavior. Blackwell, Oxford.
10. Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68: 1229-1236.
11. Crapon de Caprona MD, Ryan MJ (1990) Conspecific mate recognition in swordtails, Xiphophorus nigrensis and X. pygmaeus (Poeciliidae): olfactory and visual cues. Anim Behav 39: 290-296.
12. Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56: 2347-2358.
13. Croft CP, Albanese B, Arrowsmith BJ, Botham M, Webster M, Krause J (2003) Sex-biased movement in the guppy (Poecilia reticulata). Oecologia 137: 62-68.
14. Croft DP, Arrowsmith BJ, Webster M, Krause J (2004a) Intra-sexual preferences for familiar fish in male guppies. J Fish Biol 64: 279-283.
15. Croft DP, Krause J, James R (2004b) Social networks in the guppy (Poecilia reticulata). Proc R Soc Biol Sci Series B 271: S516-S519.
16. Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638-645.
17. 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.
18. Eikenaar C, Komdeur J, Richardson DS (2008) Natal dispersal patterns are not associated with inbreeding avoidance in the Seychelles Warbler. J Evol Biol 21: 1106-1116.
19. Fessehaye Y, Komen H, Kezk MA, van Arendonk JAM, Bovenhuis H (2007) Effects of inbreeding on survival, body weight and fluctuating asymmetry (FA) in Nile tilapia, Oreochromis niloticus. Aquaculture 264: 27-35.
20. Fisher HS, Rosenthal GG (2006) Female swordtail fish use chemical cues to select well-fed mates. Anim Behav 72: 721-725.
21. Forsberg LA, Dannewitz J, Petersson E, Grahn M (2007) Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout-females fishing for optimal MHC dissimilarity. J Evol Biol 20: 1859-1869.
22. Frommen JG, Bakker TCM (2006) Inbreeding avoidance through non-random mating in sticklebacks. Biol Lett 2: 232-235.
23. Frommen JG, Mehlis M, Brendler C, Bakker TCM (2007) Shoaling decisions in three-spined sticklebacks (Gasterosteus aculeatus)-familiarity, kinship and inbreeding. Behav Ecol Sociobiol 61: 533-539.
24. Gerlach G, Lysiak N (2006) Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim Behav 71: 1371-1377.
25. Gerlach G, Hodgins-Davis A, Avolio C, Schunter C (2008) Kin recognition in zebrafish: a 24-hour window for olfactory imprinting. Proc R Soc B Biol Sci 275: 2165-2170.
26. Gow JL (2008) The mating game: do opposites really attract? Mol Ecol 17: 1399-1400.
27. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28: 1140-1162.
28. Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56: 689-693.
29. Guevara-Fiore P, Skinner A, Watt PJ (2009) Do male guppies distinguish virgin females from recently mated ones? Anim Behav 77: 425-431.
30. Guevara-Fiore P, Stapley J, Krause J, Ramnarine IW, Watt PJ (2010) Male mate-searching strategies and female cues: how do male guppies find receptive females? Anim Behav (in press).
31. Haikola S, Singer MC, Pen I (2004) Has inbreeding depression led to avoidance of sib mating in the Glanville fritillary butterfly (Melitaea cinxia)? Evol Ecol 18: 113-120.
32. Hain TJA, Neff BD (2007) Multiple paternity and kin recognition mechanisms in a guppy population. Mol Ecol 16: 3938-3946.
33. Hansson B, Hasselquist D, Bensch S (2004) Do female great reed warblers seek extra-pair fertilizations to avoid inbreeding? Proc R Soc Lond B Biol Sci 271: S290-S292.
34. Hansson B, Jack L, Christians JK, Pemberton JM, Akesson M, Westerdahl H, Bensch S, Hasselquist D (2007) No evidence for inbreeding avoidance in a great reed warbler population. Behav Ecol 18: 157-164.
35. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31: 139-162.
36. Hoenig JM, Heisey DM (2001) The abuse of power: the pervasive fallacy of power calculations for data analysis. Am Stat 55: 19-24.
37. Houde AE (1987) Mate choice based upon naturally-occurring color-pattern variation in a guppy population. Evolution 41: 1-10.
38. Houde AE (1994) Effect of artificial selection on male color patterns on mating preference of female guppies. Proc R Soc Lond B Biol Sci 256: 125-130.
39. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton.
40. Hughes KA, Du L, Rodd FH, Reznick DN (1999) Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim Behav 58: 907-916.
41. Jansson N, Uller T, Olsson M (2005) Female dragons, Ctenophorus pictus, do not prefer scent from unrelated males. Aust J Zool 53: 279-282.
42. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75: 21-64.
43. 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.
44. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82: 265-289.
45. Keane B, Creel SR, Waser PM (1996) No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behav Ecol 7: 480-489.
46. Keller LF, Arcese P (1998) No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). Am Nat 152: 380-392.
47. Keller L, Fournier D (2002) Lack of inbreeding avoidance in the Argentine ant Linepithema humile. Behav Ecol 13: 28-31.
48. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17: 230-241.
49. Kelley JL, Graves JA, Magurran AE (1999) Familiarity breeds contempt in guppies. Nature 401: 661-662.
50. Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60: 467-475.
51. Konior M, Keller L, Radwan J (2005) Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini. Heredity 94: 577-581.
52. Lampert KP, Bernal XE, Rand AS, Mueller UG, Ryan MJ (2006) No evidence for female mate choice based on genetic similarity in the tungara frog Physalaemus pustulosus. Behav Ecol Sociobiol 59: 796-804.
53. Landry C, Garant D, Duchesne P, Bernatchez L (2001) 'Good genes as heterozygosity': the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc R Soc Lond B Biol Sci 268: 1279-1285.
54. Liley NR, Wishlow W (1974) Interaction of endocrine and experiential factors in regulation of sexual behavior in female guppy Poecilia reticulata. Behaviour 48: 185-214.
55. Lyons EJ, Frodsham AJ, Zhang L, Hill AVS, Amos W (2009) Consanguinity and susceptibility to infectious diseases in humans. Biol Lett 5: 574-576.
56. Magurran AE, Seghers BH, Shaw PW, Carvalho GR (1994) Schooling preferences for familiar fish in the guppy, Poecilia reticulata. J Fish Biol 45: 401-406.
57. Mariette M, Kelley JL, Brooks R, Evans JP (2006) The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112: 807-814.
58. Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19: 554-559.
59. McLennan DA, Ryan MJ (1997) Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Anim Behav 54: 1077-1088.
60. McLennan DA, Ryan MJ (1999) Interspecific recognition and discrimination based upon olfactory cues in northern swordtails. Evolution 53: 880-888.
61. Mehlis M, Bakker TCM, Frommen JG (2008) Smells like sib spirit: kin recognition in three-spined sticklebacks (Gasterosteus aculeatus) is mediated by olfactory cues. Anim Cogn 11: 643-650.
62. Milinski M (2003) The function of mate choice in sticklebacks: optimizing MHC genetics. J Fish Biol 63: 1-16.
63. Nakadate M, Shikano T, Taniguchi N (2003) Inbreeding depression and heterosis in various quantitative traits of the guppy, Poecilia reticulata. Aquaculture 220: 219-226.
64. Neff BD, Pitcher TE, Ramnarine IW (2008) Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol Ecol 17: 2975-2984.
65. Olsen H (1998) Present knowledge of kin discrimination in salmonids. Genetica 104: 295-299.
66. Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007) Egg production and individual genetic diversity in lesser kestrels. Mol Ecol 16: 2383-2392.
67. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108: 1-21.
68. Peters A, Michiels NK (1996) Evidence for lack of inbreeding avoidance by selective simultaneous hermaphrodite. Invertebr Biol 115: 99-103.
69. Pitcher TE, Neff BD, Rodd FH, Rowe L (2003) Multiple mating and sequential mate choice in guppies: females trade up. Proc R Soc Lond B Biol Sci 270: 1623-1629.
70. Pitcher TE, Rodd FH, Rowe L (2008) Female choice and the relatedness of mates in the guppy (Poecilia reticulata). Genetica 134: 137-146.
71. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11: 201-206.
72. R Core Development Team (2006) R: a language and environment for statistical computing. Austria, Vienna.
73. Radwan J (2003) Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90: 371-376.
74. Rätti O, Hovi M, Lundberg A, Tegelstrom H, Alatalo RV (1995) Extra-pair paternity and male characteristics in the pied flycatcher. Behav Ecol Sociobiol 37: 419-425.
75. Reusch TBH, Häberli MA, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414: 300-302.
76. Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the seychelles warbler: environment-dependent maternal effects. Evolution 58: 2037-2048.
77. Russell ST, Kelley JL, Graves JA, Magurran AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106: 520-526.
78. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20: 416-420.
79. Schjørring S, Jager I (2007) Incestuous mate preference by a simultaneous hermaphrodite with strong inbreeding depression. Evolution 61: 423-430.
80. Schmoll T, Quellmalz A, Dietrich V, Winkel W, Epplen JT, Lubjuhn T (2005) Genetic similarity between pair mates is not related to extrapair paternity in the socially monogamous coal tit. Anim Behav 69: 1013-1022.
81. Sherman CDH, Wapstra E, Uller T, Olsson M (2008) Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frog Litoria peronii. Proc R Soc B Biol Sci 275: 971-978.
82. Shikano T, Taniguchi N (2002) Heterosis for neonatal survival in the guppy. J Fish Biol 60: 715-725.
83. Shohet AJ, Watt PJ (2004) Female association preferences based on olfactory cues in the guppy, Poecilia reticulata. Behav Ecol Sociobiol 55: 363-369.
84. Stiver KA, Fitzpatrick JL, Desjardins JK, Neff BD, Quinn JS, Balshine S (2008) The role of genetic relatedness among social mates in a cooperative breeder. Behav Ecol 19: 816-823.
85. Swindell WR, Bouzat JL (2006) Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging. J Evol Biol 19: 1257-1264.
86. Szulkin M, Garant D, McCleery RH, Sheldon BC (2007) Inbreeding depression along a life-history continuum in the great tit. J Evol Biol 20: 1531-1543.
87. Thünken T, Bakker TCM, Baldauf SA, Kullmann H (2007) Active inbreeding in a cichlid fish and its adaptive significance. Curr Biol 17: 225-229.
88. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415: 71-73.
89. van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, Shaw PW (2003) Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol 16: 273-281.
90. Viken A, Fleming IA, Rosenqvist G (2006) Premating avoidance of inbreeding absent in female guppies (Poecilia reticulata). Ethology 112: 716-723.
91. Ward AJW, Hart PJB, Krause J (2004) The effects of habitat- and diet-based cues on association preferences in three-spined sticklebacks. Behav Ecol 15: 925-929.
92. Zajitschek SRK, Evans JP, Brooks R (2006) Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies. Behav Ecol 17: 911-916.