Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Significant empirical evidence has demonstrated the importance of discriminative mate choice as a mechanism to avoid inbreeding. Incestuous mating can be avoided by recognition of kin. The guppy, Poecilia reticulata, is a livebearer with a polygamous mating system and active female choice. Despite potential inbreeding costs in the guppy, Viken et al. (Ethology 112:716–723, 2006) and Pitcher et al. (Genetica 134:137–146, 2008) have found that females do not discriminate between sibs and unrelated males. However, populations experiencing different inbreeding histories can have different levels of inbreeding avoidance, and it is possible that the lack of inbreeding avoidance observed in guppies is a consequence of using outbred fish only. Here we tested the preference of female guppies with different inbreeding coefficients, for olfactory cues of males that were either unrelated but had the same inbreeding coefficient, or were related (i.e. brother) with the same inbreeding coefficient. We found no evidence that female guppies preferred unrelated males with the same inbreeding coefficient. Moreover, inbreeding level did not influence female preference for unrelated males, suggesting that inbreeding history in a population has no influence on female discrimination of unrelated males in guppies.

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

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Becher SA, Magurran AE (2004) Multiple mating and reproductive skew in Trinidadian guppies. Proc R Soc Biol Sci Series B 271:1009–1014

    Article  CAS  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 

  • 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

    Article  PubMed  Google Scholar 

  • Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65

    Article  Google Scholar 

  • Brown C, Laland KN, Krause J (2006) Fish cognition and behavior. Blackwell, Oxford

    Google Scholar 

  • Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68:1229–1236

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Croft DP, Arrowsmith BJ, Webster M, Krause J (2004a) Intra-sexual preferences for familiar fish in male guppies. J Fish Biol 64:279–283

    Article  Google Scholar 

  • Croft DP, Krause J, James R (2004b) Social networks in the guppy (Poecilia reticulata). Proc R Soc Biol Sci Series B 271:S516–S519

    Article  Google Scholar 

  • Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57:638–645

    CAS  PubMed  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 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fisher HS, Rosenthal GG (2006) Female swordtail fish use chemical cues to select well-fed mates. Anim Behav 72:721–725

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Frommen JG, Bakker TCM (2006) Inbreeding avoidance through non-random mating in sticklebacks. Biol Lett 2:232–235

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gow JL (2008) The mating game: do opposites really attract? Mol Ecol 17:1399–1400

    Article  PubMed  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56:689–693

    Article  PubMed  Google Scholar 

  • Guevara-Fiore P, Skinner A, Watt PJ (2009) Do male guppies distinguish virgin females from recently mated ones? Anim Behav 77:425–431

    Article  Google Scholar 

  • 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)

  • 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

    Article  Google Scholar 

  • Hain TJA, Neff BD (2007) Multiple paternity and kin recognition mechanisms in a guppy population. Mol Ecol 16:3938–3946

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Hoenig JM, Heisey DM (2001) The abuse of power: the pervasive fallacy of power calculations for data analysis. Am Stat 55:19–24

    Article  Google Scholar 

  • Houde AE (1987) Mate choice based upon naturally-occurring color-pattern variation in a guppy population. Evolution 41:1–10

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, Princeton

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    Article  CAS  PubMed  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 

  • Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289

    Article  PubMed  Google Scholar 

  • Keane B, Creel SR, Waser PM (1996) No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behav Ecol 7:480–489

    Article  CAS  Google Scholar 

  • Keller LF, Arcese P (1998) No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). Am Nat 152:380–392

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

    Article  Google Scholar 

  • Kelley JL, Graves JA, Magurran AE (1999) Familiarity breeds contempt in guppies. Nature 401:661–662

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lyons EJ, Frodsham AJ, Zhang L, Hill AVS, Amos W (2009) Consanguinity and susceptibility to infectious diseases in humans. Biol Lett 5:574–576

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559

    Article  PubMed  Google Scholar 

  • McLennan DA, Ryan MJ (1997) Responses to conspecific and heterospecific olfactory cues in the swordtail Xiphophorus cortezi. Anim Behav 54:1077–1088

    Article  PubMed  Google Scholar 

  • McLennan DA, Ryan MJ (1999) Interspecific recognition and discrimination based upon olfactory cues in northern swordtails. Evolution 53:880–888

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Milinski M (2003) The function of mate choice in sticklebacks: optimizing MHC genetics. J Fish Biol 63:1–16

    Article  Google Scholar 

  • Nakadate M, Shikano T, Taniguchi N (2003) Inbreeding depression and heterosis in various quantitative traits of the guppy, Poecilia reticulata. Aquaculture 220:219–226

    Article  Google Scholar 

  • Neff BD, Pitcher TE, Ramnarine IW (2008) Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol Ecol 17:2975–2984

    Article  PubMed  Google Scholar 

  • Olsen H (1998) Present knowledge of kin discrimination in salmonids. Genetica 104:295–299

    Article  CAS  PubMed  Google Scholar 

  • Ortego J, Calabuig G, Cordero PJ, Aparicio JM (2007) Egg production and individual genetic diversity in lesser kestrels. Mol Ecol 16:2383–2392

    Article  CAS  PubMed  Google Scholar 

  • Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21

    Article  Google Scholar 

  • Peters A, Michiels NK (1996) Evidence for lack of inbreeding avoidance by selective simultaneous hermaphrodite. Invertebr Biol 115:99–103

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pitcher TE, Rodd FH, Rowe L (2008) Female choice and the relatedness of mates in the guppy (Poecilia reticulata). Genetica 134:137–146

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • R Core Development Team (2006) R: a language and environment for statistical computing. Austria, Vienna

    Google Scholar 

  • Radwan J (2003) Inbreeding depression in fecundity and inbred line extinction in the bulb mite, Rhizoglyphus robini. Heredity 90:371–376

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the seychelles warbler: environment-dependent maternal effects. Evolution 58:2037–2048

    PubMed  Google Scholar 

  • Russell ST, Kelley JL, Graves JA, Magurran AE (2004) Kin structure and shoal composition dynamics in the guppy, Poecilia reticulata. Oikos 106:520–526

    Article  Google Scholar 

  • Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol 20:416–420

    Article  PubMed  Google Scholar 

  • Schjørring S, Jager I (2007) Incestuous mate preference by a simultaneous hermaphrodite with strong inbreeding depression. Evolution 61:423–430

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shikano T, Taniguchi N (2002) Heterosis for neonatal survival in the guppy. J Fish Biol 60:715–725

    Article  Google Scholar 

  • Shohet AJ, Watt PJ (2004) Female association preferences based on olfactory cues in the guppy, Poecilia reticulata. Behav Ecol Sociobiol 55:363–369

    Article  Google Scholar 

  • 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

    Article  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  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Thünken T, Bakker TCM, Baldauf SA, Kullmann H (2007) Active inbreeding in a cichlid fish and its adaptive significance. Curr Biol 17:225–229

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgements

We are very thankful to Henriette Vaagland and Gine Skjærvø for their help during the experiment; Christophe Pelabon, Geir Hysing Bolstad, Camilla Egset Kalvatn, Line Larsen and Tonje Aronsen for helpful discussions and advice; and Jessica Stapley for statistical advice. We are also grateful to three anonymous referees for their constructive comments in an earlier version of the manuscript. P. Guevara-Fiore was supported by a Dorothy Hodgkin Postgraduate Award and the Excellence Exchange Scheme of the University of Sheffield. G. Rosenqvist was supported by the Norwegain Research Council.

Author information

Authors and Affiliations

  1. Department of Animal & Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK

    Palestina Guevara-Fiore & Penelope J. Watt

  2. Department of Biology, Centre for Conservation Biology, Norwegian University of Science and Technology, Trondheim, Norway

    Gunilla Rosenqvist

Authors
  1. Palestina Guevara-Fiore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gunilla Rosenqvist
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Penelope J. Watt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Palestina Guevara-Fiore.

Additional information

Communicated by: J. Krause

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guevara-Fiore, P., Rosenqvist, G. & Watt, P.J. Inbreeding level does not induce female discrimination between sibs and unrelated males in guppies. Behav Ecol Sociobiol 64, 1601–1607 (2010). https://doi.org/10.1007/s00265-010-0973-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-0973-5

Keywords

Search

Navigation