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. 2004 Oct 7;271(1552):2035–2042. doi: 10.1098/rspb.2004.2815

Sire attractiveness influences offspring performance in guppies.

Jonathan P Evans 1, Jennifer L Kelley 1, Angelo Bisazza 1, Elisabetta Finazzo 1, Andrea Pilastro 1
PMCID: PMC1691832  PMID: 15451693

Abstract

According to the good-genes hypothesis, females choose among males to ensure the inheritance of superior paternal genes by their offspring. Despite increasing support for this prediction, in some cases differential (non-genetic) maternal effects may obscure or amplify the relationship between paternal attractiveness and offspring quality. Artificial insemination controls such effects because it uncouples mate choice from copulation, therefore denying females the opportunity of assessing male attractiveness. We adopted this technique in the live-bearing fish Poecilia reticulata and examined whether paternal coloration was associated with the behavioural performance of newborn offspring. Sexually receptive virgin females were inseminated with sperm taken individually from donor males that exhibited high variation in the area of orange pigmentation, a trait known to influence female choice in the study population. Our analysis of offspring performance focused on the anti-predator behaviour of newborn fish, including schooling by sibling pairs, the response (swimming speed) of these fishes to a simulated avian predator, and the time taken for a naive investigator to capture the offspring. Although we found no significant effect of sire coloration on either schooling or swimming speed, our analysis revealed a significant positive association between sire coloration and the ability of newborn offspring to evade capture. This finding supports the view that at least one aspect of anti-predator behaviour in newborn offspring is influenced by sire genotype, which in turn is revealed by the expression of secondary sexual traits.

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Selected References

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  1. Barber I., Arnott S. A., Braithwaite V. A., Andrew J., Huntingford F. A. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc Biol Sci. 2001 Jan 7;268(1462):71–76. doi: 10.1098/rspb.2000.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brooks R., Endler J. A. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution. 2001 May;55(5):1002–1015. doi: 10.1554/0014-3820(2001)055[1002:daissa]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  3. Brooks R., Endler J. A. Female guppies agree to differ: phenotypic and genetic variation in mate-choice behavior and the consequences for sexual selection. Evolution. 2001 Aug;55(8):1644–1655. doi: 10.1111/j.0014-3820.2001.tb00684.x. [DOI] [PubMed] [Google Scholar]
  4. Brooks R. Negative genetic correlation between male sexual attractiveness and survival. Nature. 2000 Jul 6;406(6791):67–70. doi: 10.1038/35017552. [DOI] [PubMed] [Google Scholar]
  5. CLARK E. A method for artificial insemination in viviparous fishes. Science. 1950 Dec 15;112(2920):722–723. doi: 10.1126/science.112.2920.722. [DOI] [PubMed] [Google Scholar]
  6. Cunningham E. J., Russell A. F. Egg investment is influenced by male attractiveness in the mallard. Nature. 2000 Mar 2;404(6773):74–77. doi: 10.1038/35003565. [DOI] [PubMed] [Google Scholar]
  7. Evans J. P., Magurran A. E. Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy. Proc Biol Sci. 2001 Apr 7;268(1468):719–724. doi: 10.1098/rspb.2000.1577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Evans Jonathan P., Zane Lorenzo, Francescato Samuela, Pilastro Andrea. Directional postcopulatory sexual selection revealed by artificial insemination. Nature. 2003 Jan 23;421(6921):360–363. doi: 10.1038/nature01367. [DOI] [PubMed] [Google Scholar]
  9. Gil D., Graves J., Hazon N., Wells A. Male attractiveness and differential testosterone investment in zebra finch eggs. Science. 1999 Oct 1;286(5437):126–128. doi: 10.1126/science.286.5437.126. [DOI] [PubMed] [Google Scholar]
  10. Hosken D. J., Garner T. W. J., Tregenza T., Wedell N., Ward P. I. Superior sperm competitors sire higher-quality young. Proc Biol Sci. 2003 Sep 22;270(1527):1933–1938. doi: 10.1098/rspb.2003.2443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Houde A. E., Endler J. A. Correlated Evolution of Female Mating Preferences and Male Color Patterns in the Guppy Poecilia reticulata. Science. 1990 Jun 15;248(4961):1405–1408. doi: 10.1126/science.248.4961.1405. [DOI] [PubMed] [Google Scholar]
  12. Hunt John, Bussière Luc F., Jennions Michael D., Brooks Robert. What is genetic quality? Trends Ecol Evol. 2004 Jun;19(6):329–333. doi: 10.1016/j.tree.2004.03.035. [DOI] [PubMed] [Google Scholar]
  13. Jennions M. D., Petrie M. Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc. 2000 Feb;75(1):21–64. doi: 10.1017/s0006323199005423. [DOI] [PubMed] [Google Scholar]
  14. Kirkpatrick M., Barton N. H. The strength of indirect selection on female mating preferences. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1282–1286. doi: 10.1073/pnas.94.4.1282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kokko Hanna, Brooks Robert, Jennions Michael D., Morley Josephine. The evolution of mate choice and mating biases. Proc Biol Sci. 2003 Mar 22;270(1515):653–664. doi: 10.1098/rspb.2002.2235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kozielska Magdalena, Krzemińska Alina, Radwan Jacek. Good genes and the maternal effects of polyandry on offspring reproductive success in the bulb mite. Proc Biol Sci. 2004 Jan 22;271(1535):165–170. doi: 10.1098/rspb.2003.2585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Møller A. P. Male ornament size as a reliable cue to enhanced offspring viability in the barn swallow. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6929–6932. doi: 10.1073/pnas.91.15.6929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. doi: 10.1098/rspb.1997.0099. [DOI] [PMC free article] [Google Scholar]
  19. doi: 10.1098/rspb.1999.0938. [DOI] [PMC free article] [Google Scholar]
  20. Parker Timothy H. Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus). Evolution. 2003 Sep;57(9):2157–2165. doi: 10.1111/j.0014-3820.2003.tb00393.x. [DOI] [PubMed] [Google Scholar]
  21. Pilastro Andrea, Evans Jonathan P., Sartorelli Silvia, Bisazza Angelo. Male phenotype predicts insemination success in guppies. Proc Biol Sci. 2002 Jul 7;269(1498):1325–1330. doi: 10.1098/rspb.2002.2017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pilastro Andrea, Simonato Martina, Bisazza Angelo, Evans Jonathan P. Cryptic female preference for colorful males in guppies. Evolution. 2004 Mar;58(3):665–669. [PubMed] [Google Scholar]
  23. Pitcher Trevor E., Neff Bryan D., Rodd F. Helen, Rowe Locke. Multiple mating and sequential mate choice in guppies: females trade up. Proc Biol Sci. 2003 Aug 7;270(1524):1623–1629. doi: 10.1098/rspb.2002.2280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Reinhold Klaus. Modelling the evolution of female choice strategies under inbreeding conditions. Genetica. 2002 Nov;116(2-3):189–195. [PubMed] [Google Scholar]
  25. Saino Nicola, Ferrari Raffaella Paola, Martinelli Roberta, Romano Maria, Rubolini Diego, Møller Anders Pape. Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc Biol Sci. 2002 May 22;269(1495):1005–1009. doi: 10.1098/rspb.2002.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sandvik M., Rosenqvist G., Berglund A. Male and female mate choice affects offspring quality in a sex-role-reversed pipefish. Proc Biol Sci. 2000 Nov 7;267(1458):2151–2155. doi: 10.1098/rspb.2000.1262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sheldon B. C., Arponen H., Laurila A., Crochet P. A., Merilä J. Sire coloration influences offspring survival under predation risk in the moorfrog. J Evol Biol. 2003 Nov;16(6):1288–1295. doi: 10.1046/j.1420-9101.2003.00606.x. [DOI] [PubMed] [Google Scholar]
  28. Sheldon BC. Differential allocation: tests, mechanisms and implications. Trends Ecol Evol. 2000 Oct 1;15(10):397–402. doi: 10.1016/s0169-5347(00)01953-4. [DOI] [PubMed] [Google Scholar]
  29. Shine R., Olsson M. When to be born? Prolonged pregnancy or incubation enhances locomotor performance in neonatal lizards (Scincidae). J Evol Biol. 2003 Sep;16(5):823–832. doi: 10.1046/j.1420-9101.2003.00600.x. [DOI] [PubMed] [Google Scholar]
  30. Welch A. M., Semlitsch R. D., Gerhardt H. C. Call duration as an indicator of genetic quality in male gray tree frogs. Science. 1998 Jun 19;280(5371):1928–1930. doi: 10.1126/science.280.5371.1928. [DOI] [PubMed] [Google Scholar]
  31. Zahavi A. Mate selection-a selection for a handicap. J Theor Biol. 1975 Sep;53(1):205–214. doi: 10.1016/0022-5193(75)90111-3. [DOI] [PubMed] [Google Scholar]
  32. van Oosterhout C., Trigg R. E., Carvalho G. R., Magurran A. E., Hauser L., Shaw P. W. Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J Evol Biol. 2003 Mar;16(2):273–281. doi: 10.1046/j.1420-9101.2003.00511.x. [DOI] [PubMed] [Google Scholar]

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