Inbreeding depression, or the reduction in fitness due to mating between close relatives, is a key issue in biology today. Inbreeding negatively affects many fitness-related traits, including survival and reproductive success. Despite this, very few studies have quantified the effects of inbreeding on vertebrate gamete traits under controlled breeding conditions using a full-sib mating approach. Here, we provide comprehensive evidence for the negative effect of inbreeding on sperm traits in a bird, the zebra finch Taeniopygia guttata. We compared sperm characteristics of both inbred (pedigree F = 0.25) and outbred (pedigree F = 0) individuals from two captive populations, one domesticated and one recently wild-derived, raised under standardized conditions. As normal spermatozoa morphology did not differ consistently between inbred and outbred individuals, our study confirms the hypothesis that sperm morphology is not particularly susceptible to inbreeding depression. Inbreeding did, however, lead to significantly lower sperm motility and a substantially higher percentage of abnormal spermatozoa in ejaculate. These results were consistent across both study populations, confirming the generality and reliability of our findings.

Department of Behavioural Ecology and Evolutionary Genetics Max Planck Institute for Ornithology Eberhard Gwinner Strasse 7 82319 Seewiesen Germany

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic v v i Květná 8CZ 603 65 Brno Czech Republic; Charles University Prague Faculty of Sciences Department of Zoology Viničná 7CZ 12844 Prague Czech Republic

Institute of Vertebrate Biology Academy of Sciences of the Czech Republic v v i Květná 8CZ 603 65 Brno Czech Republic; Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 267 2CZ 61137 Brno Czech Republic

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Ala‐Honkola, O. , Hosken D. J., Manier M. K., Lüpold S., Droge‐Young E. M., Berben K. S., et al. 2013. Inbreeding reveals mode of past selection on male reproductive characters in Drosophila melanogaster . Ecol. Evol. 3:2089–2102. PubMed PMC

Bates, D. , Maechler M., and Bolker B.. 2013. lme4: Linear mixed‐effects models using S4 classes. (R package version 0.999999‐2 ed. http://CRAN.R-project.org/package=lme4).

Bennison, C. , Hemmings N., Slate J., and Birkhead T.. 2015. Long sperm fertilize more eggs in a bird. Proc. Biol. Sci. 282:20141897. PubMed PMC

Bijlsma, R. , Bundgaard J., and Boerema A. C.. 2000. Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila . J. Evol. Biol. 13:502–514.

Birkhead, T. R. 2010. How stupid not to have thought of that: post‐copulatory sexual selection. J. Zool. 281:78–93.

Birkhead, T. R. , Pellatt E. J., Brekke P., Yeates R., and Castillo‐Juarez H.. 2005. Genetic effects on sperm design in the zebra finch. Nature 434:383–387. PubMed

Bolund, E. , Martin K., Kempenaers B., and Forstmeier W.. 2010. Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim. Behav. 79:947–955.

Briskie, J. V. , Montgomerie R., and Birkhead T. R.. 1997. The evolution of sperm size in birds. Evolution 51:937–945. PubMed

Calhim, S. , Immler S., and Birkhead T. R.. 2007. Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One 2:e413. PubMed PMC

Charlesworth, D. , and Charlesworth B.. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237–268.

Charlesworth, D. , and Willis J. H.. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10:783–796. PubMed

Crnokrak, P. , and Roff D. A.. 1999. Inbreeding depression in the wild. Heredity 83:260–270. PubMed

Denk, A. G. , Holzmann A., Peters A., Vermeirssen E. L. M., and Kempenaers B.. 2005. Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav. Ecol. 16:825–833.

van Eldik, P. , van der Waaij E. H., Ducro B., Kooper A. W., Stout T. A. E., and Colenbrander B.. 2006. Possible negative effects of inbreeding on semen quality in Shetland pony stallions. Theriogenology 65:1159–1170. PubMed

Falconer, D. S. , and Mackay T. F. C.. 1996. Introduction to quantitative genetics, 4th edn. Longman, Harlow, UK: 480 pp.

Fanelli, D. 2011. Negative results are disappearing from most disciplines and countries. Scientometrics 90:891–904.

Fitzpatrick, J. L. , and Evans J. P.. 2009. Reduced heterozygosity impairs sperm quality in endangered mammals. Biol. Lett. 5:320–323. PubMed PMC

Forstmeier, W. , Segelbacher G., Mueller J. C., and Kempenaers B.. 2007. Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol. Ecol. 16:4039–4050. PubMed

Fritzsche, P. , Neumann K., Nasdal K., and Gattermann R.. 2006. Differences in reproductive success between laboratory and wild‐derived golden hamsters Mesocricetus auratus as a consequence of inbreeding. Behav. Ecol. Sociobiol. 60:220‐226.

Frankham, R. 2005. Genetics and extinction. Biol. Conserv. 126:131–140.

Gage, M. J. G. , Surridge A. K., Tomkins J. L., Green E., Wiskin L., Bell D. J., et al. 2006. Reduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus . Curr. Biol. 16:612–617. PubMed

Gasparini, C. , Devigili A., Dosselli R., and Pilastro A.. 2013. Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits. Ecol. Evol. 3:4940–4953. PubMed PMC

Gomendio, M. , Cassinello J., and Roldan E. R.. 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. Biol. Sci. 267:875–882. PubMed PMC

Griffith, S. C. , Owens I. P. F., and Thuman K. A.. 2002. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11:2195–2212. PubMed

Helfenstein, F. , Losdat S., Møller A. P., Blount J. D., and Richner H.. 2010. Sperm of colourful males are better protected against oxidative stress. Ecol. Lett. 13:213–222. PubMed

Ihle, M. , Kempenaers B., and Forstmeier W.. 2013. Does hatching failure breed infidelity? Behav. Ecol. 24:119–127.

Immler, S. , Calhim S., and Birkhead T. R.. 2008. Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538–1543. PubMed

Immler, S. , Pitnick S., Parker G. A., Durrant K. L., Lüpold S., Calhim S., et al. 2011. Resolving variation in the reproductive tradeoff between sperm size and number. Proc. Natl. Acad. Sci. U S A 108:5325–5330. PubMed PMC

Keller, L. F. , and Waller D. M.. 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241.

Kleven, O. , Laskemoen T., Fossøy F., Robertson R. J., and Lifjeld J. T.. 2008. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62:494–499. PubMed

Knief, U. , Hemmrich‐Stanisak G., Wittig M., Franke A., Griffith S. C., Kempenaers B., et al. 2015. Quantifying realized inbreeding in wild and captive animal populations. Heredity 114:397–403. PubMed PMC

König, S. , Tsehay F., Sitzenstock F., von Borstel U. U., Schmutz M., Preisinger R., et al. 2010. Evaluation of inbreeding in laying hens by applying optimum genetic contribution and gene flow theory. Poultry Sci. 89:658–667. PubMed

Laskemoen, T. , Kleven O., Fossøy F., Robertson R. J., Rudolfsen G., and Lifjeld J. T.. 2010. Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor . Behav. Ecol. Sociobiol. 64:1473–1483.

Leberg, P. L. , and Firmin B. D.. 2008. Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol. Ecol. 17:334–343. PubMed

Lifjeld, J. T. , Laskemoen T., Kleven O., Albrecht T., and Robertson R. J.. 2010. Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One 5:e13456. PubMed PMC

Losdat, S. , Chang S.‐M., and Reid J. M.. 2014. Inbreeding depression in male gametic performance. J. Evol. Biol. 27:992–1011. PubMed

Lynch, M. , and Walsh B.. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MA: 980 pp.

Makina, S. O. , Muchadeyi F. C., van Marle‐Köster E., MacNeil M. D., and Maiwashe A.. 2014. Genetic diversity and population structure among six cattle breeds in South Africa using a whole genome SNP panel. Front. Genet. 5:333. PubMed PMC

Malo, A. F. , Garde J. J., Soler A. J., García A. J., Gomendio M., and Roldan E. R. S.. 2005. Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol. Reprod. 72:822–829. PubMed

Maximini, L. , Fuerst‐Waltl B., Gredler B., and Baumung R.. 2011. Inbreeding depression on semen quality in Austrian dual‐purpose simmental bulls. Reprod. Domest. Anim. 46:e102–e104. PubMed

Mehlis, M. , Frommen J. G., Rahn A. K., and Bakker T. C. M.. 2012. Inbreeding in three‐spined sticklebacks (Gasterosteus aculeatus L.): effects on testis and sperm traits. Biol. J. Linnean Soc. 107:510–520.

Michalczyk, L. , Martin O. Y., Millard A. L., Emerson B. C., and Gage M. J. G.. 2010. Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum . Proc. Biol. Sci. 277:3483–3491. PubMed PMC

Nakagawa, S. , and Schielzeth H.. 2010. Repeatability for Gaussian and non‐Gaussian data: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 85:935–956. PubMed

Nayernia, K. , Adham I., Kremling H., Reim K., Schlicker M., Schlüter G., et al. 1996. Stage and developmental specific gene expression during mammalian spermatogenesis. Int. J. Dev. Biol. 40:379–383. PubMed

Parker, G. A. 1982. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theoret. Biol. 96:281–294. PubMed

Parker, G. A. 1998. Sperm competition and the evolution of ejaculates: Towards a theory base Pp. 3–54 in Birkhead T. R. and Møller A. P., eds. Sperm competition and sexual selection. Academic Press, London.

Pizzari, T. , and Parker G. A.. 2009. Sperm competition and sperm phenotype Pp. 207–246 in Birkhead T. R., Hosken D. J. and Pitnick S., eds. Sperm biology: an evolutionary. Academic Press, Oxford, U.K.

Pizzari, T. , Worley K., Burke T., and Froman D. P.. 2008. Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol. Biol. 8:332. PubMed PMC

R Development Core Team . 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria: URL http://www.R-project.org.

Roldan, E. R. , Murase T., and Shi Q. X.. 1994. Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science 266:1578–1581. PubMed

Rowe, L. , and Houle D.. 1996. The Lek paradox and the capture of genetic variance by condition dependent traits. Proc. Biol. Sci. 263:1415–1421.

Saacke, R. G. , Nadir S., and Nebel R. L.. 1994. Relationship of semen quality to sperm transport, fertilization, and embryo quality in ruminants. Theriogenology 41:45–50.

Saccheri, I. , Kuussaari M., Kankare M., Vikman P., Fortelius W., and Hanski I.. 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494.

Sewalem, A. , Johansson K., Wilhelmson M., and Lillpers K.. 1999. Inbreeding and inbreeding depression on reproduction and production traits of White Leghorn lines selected for egg production traits. Br. Poult. Sci. 40:203–208. PubMed

Slate, J. , and Pemberton J.. 2006. Does reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)? Curr. Biol. 16: R790–R791; author reply R791–792. PubMed

Snook, R. R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20:46–53. PubMed

Wildt, D. E. , Baas E. J., Chakraborty P. K., Wolfle T. L., and Stewart A. P.. 1982. Influence of inbreeding on reproductive performance, ejaculate quality and testicular volume in the dog. Theriogenology 17:445–452. PubMed

Wright, L. I. , Tregenza T., and Hosken D. J.. 2008. Inbreeding, inbreeding depression and extinction. Conserv. Genet. 9:833–843.

Zajitschek, S. R. K. , Lindholm A. K., Evans J. P., and Brooks R. C.. 2009. Experimental evidence that high levels of inbreeding depress sperm competitiveness. J. Evol. Biol. 22:1338–1345. PubMed

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