Inbreeding reveals mode of past selection on male reproductive characters in Drosophila melanogaster
Version of Record online: 3 JUN 2013
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Ecology and Evolution
Volume 3, Issue 7, pages 2089–2102, July 2013
How to Cite
Ecology and Evolution 2013; 3(7): 2089–2102
- Issue online: 10 JUL 2013
- Version of Record online: 3 JUN 2013
- Manuscript Accepted: 6 MAY 2013
- Manuscript Revised: 3 MAY 2013
- Manuscript Received: 25 MAR 2013
- Academy of Finland. Grant Numbers: 135684, 250999
- Ella and Georg Ehrnrooth's Foundation
- U.S. National Science Foundation. Grant Numbers: DEB-0814732, DEB-1021240
- Swiss National Science Foundation. Grant Number: PBSKP3_130878
- 2009. Strong inbreeding depression in male mating behaviour in a poeciliid fish. J. Evol. Biol. 22:1396–1406. , , , and .
- 2011. No evidence for postcopulatory inbreeding avoidance in Drosophila melanogaster. Evolution 65:2699–2705. , , , and .
- 1997. Rearing in different light regimes affects courtship behaviour in Drosophila melanogaster. Anim. Behav. 53:25–38. , , and .
- 1998. Cryptic female choice: criteria for establishing female sperm choice. Evolution 52:1212–1218.
- 2004. Nontransitivity of paternity in a bird. Evolution 58:416–420. , , , , and .
- 2006. Intensity of sexual selection along the anisogamy-isogamy continuum. Nature 441:742–745. , and .
- 2007. Complex interactions with females and rival males limit the evolution of sperm offence and defence. Proc. R. Soc. Lond. B 274:1779–1788. , , , , and .
- 2010. Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim. Behav. 79:947–955. , , , and .
- 2011. Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav. Ecol. Sociobiol. 65:813–821. , , and .
- 1981. Genetic variation and genetic load due to the male reproductive component of fitness in Drosophila. Genetics 97:719–730.
- 1972. Dynamics of polymorphisms. 1. Selection components in an experimental population of Drosophila melanogaster. Genetics 71:439–460. , and .
- 2000. The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster. Proc. R. Soc. Lond. B 267:1097–1105. , , , and .
- 2009. Fundamental concepts in genetics: the genetics of inbreeding depression. Nat. Rev. Gen. 10:783–796. , and .
- 2001. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98:1671–1675. , , and .
- 2002. Sperm competition and the maintenance of polymorphism. Heredity 88:148–153.
- 1998. Female genotypes affect sperm displacement in Drosophila. Genetics 149:1487–1493. , and .
- 1999. Female × male interactions in Drosophila sperm competition. Science 283:217–220. , , and .
- 1999. A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution 53:1288–1292. , and .
- 2009. Analysis of longitudinal data. Oxford University Press, Oxford, U.K. , , , and .
- 1996. Female control: sexual selection by cryptic female choice. Princeton Univ. Press, Princeton, NJ.
- 2006. Possible negative effects of inbreeding on semen quality in Shetland pony stallions. Theriogenology 65:1159–1170. , , , , , and .
- 2004. Inbreeding depression in Nigella degenii (Ranunculaceae): fitness components compared with morphological and phenological characters. Int. J. Plant Sci. 165:1055–1061. , and .
- 2010. Sex-specific effects of inbreeding in wild-caught Drosophila melanogaster under benign and stressful conditions. J. Evol. Biol. 23:2309–2323. , and .
- 1996. Introduction to quantitative genetics. Longman, London, U.K. , and .
- 2009. Reduced heterozygosity impairs sperm quality in endangered mammals. Biol. Lett. 5:320–323. , and .
- 2007. Associations between sperm competition and natural variation in male reproductive genes on the third chromosome of Drosophila melanogaster. Genetics 176:1245–1260. , , and .
- 2002. Introduction to conservation genetics. Cambridge Univ. Press, Cambridge, U.K. , , and .
- 2010. Sperm competitive ability and indices of lifetime reproductive success. Evolution 64:2746–2757. , , , , and .
- 2004. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14:44–47. , , , , , and .
- 2006. Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Curr. Biol. 16:612–617. , , , , , , et al.
- 2005. Sperm viability matters in insect sperm competition. Curr. Biol. 15:271–275. , and .
- 2000. A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proc. R. Soc. Lond. B 267:875–882. , , and .
- 2008. Attractive males have greater success in sperm competition. Curr. Biol. 18:R553–R554. , , , , and .
- 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195–204.
- 1995. The inbreeding decline and average dominance of genes affecting male life-history characters in Drosophila melanogaster. Genet. Res. 65:41–52.
- 1997. Quantitative genetics of sperm precedence in Drosophila melanogaster. Genetics 145:139–151.
- 2009. Females prefer the scent of outbred males: good-genes-as-heterozygosity? BMC Evol. Biol. 9:104. , , , and .
- 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc. Natl Acad. Sci. USA 108:5325–5330. , , , , , , et al.
- 2003. Captivity masks inbreeding effects on male mating success in butterflies. Nature 424:191–194. , and .
- 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241. , and .
- 2010. Inbreeding, energy use and sexual signaling. Evol. Ecol. 24:761–772. , and .
- 2012. Inbreeding depression in the effects of body mass on energy use. Biol. J. Linn. Soc. 105:309–317. , and .
- Manipulating genetic architecture to reveal fitness relationships. Proc. Peerage Sci. , , and . in press.
- 2005. Effect of inbreeding and heritability of sperm competition success in the bulb mite Rhizoglyphus robini. Heredity 94:577–581. , , and .
- 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40. , and .
- 2011. Male Drosophila melanogaster adjust ejaculate size based on female mating status, fecundity, and age. Behav. Ecol. 22:184–191. , , , , and .
- 2012. How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr. Biol. 22:1667–1672. , , , , , , et al.
- 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Inc., Sunderland, MA. , and .
- 1985. A quantitative genetic analysis of fitness and its components in Drosophila melanogaster. Genet. Res. 47:59–70.
- 2011. Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females. Heredity 106:994–1002. , and .
- 2010. Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328:354–357. , , , , , and .
- 2013. Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution. doi: 10.1111/evo.12117 , , , , , , et al.
- 2002. The effects of inbreeding on testicular sperm concentration in Peromyscus polionotus. Reprod. Fertil. Dev. 14:63–67. , and .
- 2006. The effects of inbreeding on male courtship behaviour and coloration in guppies. Ethology 112:807–814. , , , and .
- 1991. Mating propensity and courtship behavior in serially bottlenecked lines of the housefly. Evolution 45:293–306. , and .
- 2012. Inbreeding in three-spined sticklebacks (Gasterosteus aculeatus L.): effects on testis and sperm traits. Biol. J. Linn. Soc. 107:510–520. , , , and .
- 2010. Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proc. R. Soc. Lond. B 277:3483–3491. , , , , and .
- 2002. Sperm-female coevolution in Drosophila. Science 298:1230–1233. , and .
- 1993. Inbreeding depression and male mating behavior in Drosophila melanogaster. Genetica 88:29–36. , , and .
- 2005. Patterns of sperm precedence are not affected by female mating history in Drosophila melanogaster. Evolution 59:2608–2615. , , and .
- 2008. Hemiclonal analysis reveals significant genetic, environmental and genotype × environment effects on sperm size in Drosophila melanogaster. J. Evol. Biol. 21:1692–1702. , , and .
- 2006. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133:42–51. , , , , , and .
- 2011. Male attractiveness, fertility and susceptibility to oxidative stress are influenced by inbreeding in Drosophila simulans. J. Evol. Biol. 24:363–371. , , , , and .
- 2003. Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J. Evol. Biol. 16:273–281. , , , , , and .
- 2003. Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Mol. Ecol. 12:485–492. , , , and .
- 1970. Sperm competition and its evolutionary consequences in insects. Biol. Rev. 45:525–567.
- 1985. Male mating success and fertility in Drosophila melanogaster. Genet. Res. 46:279–285. , , and .
- 2006. Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60:2064–2080. , , , and .
- 1996. Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148:57–80.
- 2000. Criteria for demonstrating female sperm choice. Evolution 54:1052–1056. , and .
- 1994. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc. Natl Acad. Sci. USA 91:9277–9281. , and .
- 1995. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc. Natl Acad. Sci. USA 92:10614–10618. , , and .
- 1999. Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53:1804–1822. , , and .
- 2003. Ejaculate-female coevolution in Drosophila mojavensis. Proc. R. Soc. Lond. B 270:1507–1512. , , , and .
- 2009a. Sperm morphological diversity. Pp. 69–149 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology: an evolutionary perspective. Elsevier, London, U.K. , , and .
- 2009b. Ejaculate-female and sperm-female interactions. Pp. 247–304 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology: an evolutionary perspective. Elsevier, London, U.K. , , and .
- 2009. Sperm competition and sperm phenotype. Pp. 207–245 in T. R. Birkhead, D. J. Hosken, and S. Pitnick, eds. Sperm biology: an evolutionary perspective. Elsevier, London, U.K. , and .
- 2012. Inbreeding affects sexual signalling in males but not females of Tenebrio molitor. Biol. Lett. 8:423–425. , , , and .
- 1971a. Relation between fitness components and population prediction in Drosophila. 1. Estimation of fitness components. Genetics 68:127–149.
- 1971b. Relation between fitness components and population prediction in Drosophila. 2. Population prediction. Genetics 68:151–167.
- R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. Available at http://www.R-project.org (accessed 24 May 2013).
- 2007. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr. Comp. Biol. 47:427–445. , and .
- 1999. Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim. Behav. 58:649–657. , , and .
- 1956. The effect of selection against extreme deviants based on deviation or on homozygosis. J. Genet. 54:236–248.
- 2009. No evidence for optimal fitness at intermediate levels of inbreeding in Drosophila melanogaster. Biol. J. Linn. Soc. 98:501–510. , , and .
- 1997. Evolutionary quantitative genetics. Chapman & Hall, New York.
- 1998. Effects of inbreeding on morphological and life history traits of the sand cricket, Gryllus firmus. Heredity 81:28–37.
- 1998. Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B 265:243–248. , , , and .
- 2010. Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate. Proc. R. Soc. Lond. B 277:2541–2546. , , , , and .
- 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494. , , , , , and .
- 1984. The effect of inbreeding on competitive male mating ability in Drosophila melanogaster. Genetics 106:601–612.
- 2011. Inbreeding depression in the competitive fertilization success of male crickets. J. Evol. Biol. 24:415–421.
- 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20:46–53.
- 2004. Sperm death and dumping in Drosophila. Nature 428:939–941. , and .
- Statistical Consulting Group. Statistical computing seminars, repeated measures analysis with R. Academic Technology Services, Statistical Consulting Group, UCLA, CA. Available at http://www.ats.ucla.edu/stat/r/seminars/repeated_measures/repeated_measures.htm (accessed 15 January 2013).
- 2008. Sexual selection and female fitness in Drosophila simulans. Behav. Ecol. Sociobiol. 62:721–728. , , and .
- 1997. Retrospective power analysis. Conserv. Biol. 11:276–280.
- 2009. Inbreeding effects on sperm production in clam shrimp (Eulimnadia texana). Evol. Ecol. Res. 11:125–134. , , , and .
- 1982. Influence of inbreeding on reproductive performance, ejaculate quality and testicular volume in the dog. Theriogenology 17:445–452. , , , , and .
- 1997. Female genotype affects male success in sperm competition. Proc. R. Soc. Lond. B 264:1491–1495. , , , and .
- 2008. Inbreeding, inbreeding depression and extinction. Conserv. Genet. 9:833–843. , , and .
- 2010. Inbreeding depression in male traits and preference for outbred males in Poecilia reticulata. Behav. Ecol. 21:884–891. , and .
- 2009. Experimental evidence that high levels of inbreeding depress sperm competitiveness. J. Evol. Biol. 22:1338–1345. , , , and .
- 1999. Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ.
- 2009. Mixed effects models and extensions in ecology with R. Springer, New York, NY. , , , , and .