Studies concerning the relationships between sperm size and velocity at the intraspecific level are quite limited and often yielded contradictory results across the animal kingdom. Intramale variation in sperm size may represent a meaningful factor to predict sperm velocity, due to its relationship with the level of sperm competition among related taxa. Because sperm phenotype is under post-copulatory sexual selection, we hypothesized that a reduced intramale variation in sperm size is associated with sperm competitiveness in red deer. Our results show that low variation in sperm size is strongly related to high sperm velocity and normal sperm morphology, which in turn are good predictors of male fertility in this species. Furthermore, it is well known that the red deer show high variability in testicular mass but there is limited knowledge concerning the significance of this phenomenon at intraspecific level, even though it may reveal interesting processes of sexual selection. Thereby, as a preliminary result, we found that absolute testes mass is negatively associated with intramale variation in sperm size. Our findings suggest that sperm size variation in red deer is under a strong selective force leading to increase sperm function efficiency, and reveal new insights into sexual selection mechanisms.

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Prague Czech Republic

SaBio IREC Albacete Spain

SaBio IREC Albacete Spain ; Department of Animal Science and Food Processing Faculty of Tropical AgriSciences Czech University of Life Sciences Prague Prague Czech Republic

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Birkhead TR, Immler S. Making sperm: design, quality control and sperm competition. Society of Reproduction and Fertility Supplement. 2007;65:175–181. PubMed

Birkhead TR, Møller AP. Sperm competition and sexual selection. London: Academic Press; 1998.

Blengini CS, Sergio N, Gabriela C, Giojalas LC, Margarita C. Variability in sperm form and function in the context of sperm competition risk in two Tupinambis lizards. Ecology and Evolution. 2014;4:4080–4092. doi: 10.1002/ece3.1262. PubMed DOI PMC

Calhim S, Double MC, Margraf N, Birkhead TR, Cockburn A. Maintenance of sperm variation in a highly promiscuous wild bird. PLoS ONE. 2011;6:e1478. doi: 10.1371/journal.pone.0028809. PubMed DOI PMC

Clutton-Brock TH, Guinness FE, Albon SD. Red deer: behaviour and ecology of two sexes. Chicago: Chicago University Press; 1982.

Cramer ERA, Laskemoen T, Stensrud E, Rowe M, Haas F, Lifjeld JT, Sætre G, Johnsen A. Morphology-function relationships and repeatability in the sperm of passer sparrows. Journal of Morphology. 2014;8:1–8. doi: 10.1002/jmor.20346. PubMed DOI

Cui KH. Size differences between human X and Y spermatozoa and prefertilization diagnosis. Molecular Human Reproduction. 1997;3:61–67. doi: 10.1093/molehr/3.1.61. PubMed DOI

Cui KH, Matthews CD. X larger than Y. Nature. 1993;366:117–118. doi: 10.1038/366117b0. PubMed DOI

Domínguez-Rebolledo AE, Fernández-Santos MR, Bisbal A, Ros-Santaella JL, Ramón M, Carmona M, Martínez-Pastor F, Garde JJ. Improving the effect of incubation and oxidative stress on thawed spermatozoa from red deer by using different antioxidant treatments. Reproduction, Fertility, and Development. 2010;22:856–870. doi: 10.1071/RD09197. PubMed DOI

Domínguez-Rebolledo AE, Martínez-Pastor F, Bisbal AF, Ros-Santaella JL, García-Álvarez O, Maroto-Morales A, Soler AJ, Garde JJ, Fernández-Santos MR. Response of thawed epididymal red deer spermatozoa to increasing concentrations of hydrogen peroxide, and importance of individual male variability. Reproduction in Domestic Animals. 2011;46:393–403. doi: 10.1111/j.1439-0531.2010.01677.x. PubMed DOI

Firman RC, Simmons LW. Sperm midpiece length predicts sperm swimming velocity in house mice. Biology Letters. 2010;6:513–516. doi: 10.1098/rsbl.2009.1027. PubMed DOI PMC

Fitzpatrick JL, Baer B. Polyandry reduces sperm length variation in social insects. Evolution. 2011;65:3006–3012. doi: 10.1111/j.1558-5646.2011.01343.x. PubMed DOI

Fitzpatrick JL, Lüpold S. Sexual selection and the evolution of sperm quality. Molecular Human Reproduction. 2014;0:1–10. doi: 10.1093/molehr/gau067. PubMed DOI

García-González F, Simmons LW. Sperm viability matters in insect sperm competition. Current Biology. 2005;15:271–275. doi: 10.1016/j.cub.2005.01.032. PubMed DOI

Gomendio M, Malo AF, Soler AJ, Fernández-Santos MR, Esteso MC, García AJ, Roldan ERS, Garde J. Male fertility and sex ratio at birth in red deer. Science. 2006;314:1445–1447. doi: 10.1126/science.1133064. PubMed DOI

Gómez Montoto L, Magaña C, Tourmente M, Martín-Coello J, Crespo C, Luque-Larena JJ, Gomendio M, Roldan ERS. Sperm competition, sperm numbers and sperm quality in muroid rodents. PLoS ONE. 2011;6:e1478. doi: 10.1371/journal.pone.0018173. PubMed DOI PMC

Griswold MD. Perspective on the function of Sertoli cells. In: Skinner MK, Griswold MD, editors. Sertoli cell biology. San Diego: Elsevier Academic Press; 2004. pp. 15–18.

Guinness F, Lincoln GA, Short RV. Reproductive cycle of female red deer, Cervus elaphus L. Journal of Reproduction and Fertility. 1971;27:427–438. doi: 10.1530/jrf.0.0270427. PubMed DOI

Helfenstein F, Podevin M, Richner H. Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behavioral Ecology and Sociobiology. 2009;64:557–565. doi: 10.1007/s00265-009-0871-x. DOI

Humphries S, Evans JP, Simmons LW. Sperm competition: linking form to function. BMC Evolutionary Biology. 2008;8:319. doi: 10.1186/1471-2148-8-319. PubMed DOI PMC

Immler S. Sperm competition and sperm cooperation: the potential role of diploid and haploid expression. Reproduction. 2008;135:275–283. doi: 10.1530/REP-07-0482. PubMed DOI

Immler S, Calhim S, Birkhead TR. Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution. 2008;62:1538–1543. doi: 10.1111/j.1558-5646.2008.00393.x. PubMed DOI

Jarnemo A. Male red deer (Cervus elaphus) dispersal during the breeding season. Journal of Ethology. 2011;29:329–336. doi: 10.1007/s10164-010-0262-9. DOI

Kelly CD. Sperm investment in relation to weapon size in a male trimorphic insect? Behavioral Ecology. 2008;19:1018–1024. doi: 10.1093/beheco/arn058. DOI

Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT. Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution. 2009;63:2466–2473. doi: 10.1111/j.1558-5646.2009.00725.x. PubMed DOI

Kleven O, Laskemoen T, Fossøy F, Robertson RJ, Lifjeld JT. Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution. 2008;62:494–499. doi: 10.1111/j.1558-5646.2007.00287.x. PubMed DOI

Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, De Lope F, Hermosell IG, Johannessen LE, Kleven O, Marzal A, Mousseau TA, Møller AP, Robertson RJ, Rudolfsen G, Saino N, Vortman Y, Lifjeld JT. Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behavioral Ecology and Sociobiology. 2013;67:301–309. doi: 10.1007/s00265-012-1450-0. DOI

Liao WB, Mi ZP, Li CL, Wei SC, Wu H. Sperm traits in relation to male amplexus position in the Omei treefrog Rhacophorus omeimontis, a species with group spawning. The Herpetological Journal. 2013;23:17–21.

Lüpold S. Ejaculate quality and constraints in relation to sperm competition levels among eutherian mammals. Evolution. 2013;67:3052–3060. doi: 10.1111/evo.12132. PubMed DOI

Lüpold S, Calhim S, Immler S, Birkhead TR. Sperm morphology and sperm velocity in passerine birds. Proceedings of the Royal Society B. 2009a;276:1175–1181. doi: 10.1098/rspb.2008.1645. PubMed DOI PMC

Lüpold S, Linz GM, Rivers JW, Westneat DF, Birkhead TR. Sperm competition selects beyond relative testes size in birds. Evolution. 2009b;63:391–402. doi: 10.1111/j.1558-5646.2008.00571.x. PubMed DOI

Malo AF, Garde JJ, Soler AJ, García AJ, Gomendio M, Roldan ERS. Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biology of Reproduction. 2005b;72:822–829. doi: 10.1095/biolreprod.104.036368. PubMed DOI

Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS. Sperm design and sperm function. Biology Letters. 2006;2:246–249. doi: 10.1098/rsbl.2006.0449. PubMed DOI PMC

Malo AF, Roldan ERS, Garde J, Soler AJ, Gomendio M. Antlers honestly advertise sperm production and quality. Proceedings of the Royal Society B. 2005a;272:149–157. doi: 10.1098/rspb.2004.2933. PubMed DOI PMC

Martínez-Pastor F, Guerra C, Kaabi M, Garcia-Macias V, De Paz P, Alvarez M, Herraez P, Anel L. Season effect on genitalia and epididymal sperm from Iberian red deer, roe deer and Cantabrian chamois. Theriogenology. 2005;63:1857–1875. doi: 10.1016/j.theriogenology.2004.08.006. PubMed DOI

Merilä J, Sheldon BC. Testis size variation in the greenfinch Carduelis chloris: relevance for some recent models of sexual selection. Behavioral Ecology and Sociobiology. 1999;45:115–123. doi: 10.1007/s002650050545. DOI

Mossman J, Pearson JT, Moore HD, Pacey A. Variation in mean human sperm length is linked with semen characteristics. Human Reproduction. 2013;28:22–32. doi: 10.1093/humrep/des382. PubMed DOI

Parker GA. Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP, editors. Sperm competition and sexual selection. London: Academic Press; 1998. pp. 3–54.

Pemberton JM, Albon SD, Guinness FE, Clutton-Brock TH, Dover GA. Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behavioral Ecology. 1992;3:66–75. doi: 10.1093/beheco/3.1.66. DOI

Pérez-González J, Carranza J. Female aggregation interacts with population structure to influence the degree of polygyny in red deer. Animal Behaviour. 2011;82:957–970. doi: 10.1016/j.anbehav.2011.07.023. DOI

Pintus E, Ros-Santaella JL, Garde JJ. Beyond testis size: links between spermatogenesis and sperm traits in a seasonal breeding mammal. PLoS ONE. 2015;10:e1478. doi: 10.1371/journal.pone.0139240. PubMed DOI PMC

Pitnick S, Hosken DJ, Birkhead TR. Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Oxford: Academic Press; 2009. pp. 69–149.

Pizzari T, Parker GA. Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S, editors. Sperm biology: an evolutionary perspective. Oxford: Academic Press; 2009. pp. 207–245.

Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K. Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proceedings of the Royal Society B. 2003;270:633–640. doi: 10.1098/rspb.2002.2268. PubMed DOI PMC

Ramm SA, Stockley P. Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biology Letters. 2010;6(2):219–221. doi: 10.1098/rsbl.2009.0635. PubMed DOI PMC

Ramón M, Soler AJ, Ortiz JA, García-Alvarez O, Maroto-Morales A, Roldan ERS, Garde JJ. Sperm population structure and male fertility: an intraspecific study of sperm design and velocity in red deer. Biology of Reproduction. 2013;89:110. doi: 10.1095/biolreprod.113.112110. PubMed DOI

Ros-Santaella JL, Domínguez-Rebolledo AE, Garde JJ. Sperm flagellum volume determines freezability in red deer spermatozoa. PLoS ONE. 2014;9:e1478. doi: 10.1371/journal.pone.0112382. PubMed DOI PMC

Rowe M, Pruett-Jones S. Sperm competition selects for sperm quantity and quality in the australian Maluridae. PLoS ONE. 2011;6(1):e1478. doi: 10.1371/journal.pone.0015720. PubMed DOI PMC

Šandera M, Albrecht T, Stopka P. Variation in apical hook length reflects the intensity of sperm competition in murine rodents. PLoS ONE. 2013;8:e1478. doi: 10.1371/journal.pone.0068427. PubMed DOI PMC

Schulte-Hostedde AI, Millar JS. Intraspecific variation of testis size and sperm length in the yellow-pine chipmunk (Tamias amoenus): implications for sperm competition and reproductive success. Behavioral Ecology and Sociobiology. 2004;55:272–277. doi: 10.1007/s00265-003-0707-z. DOI

Simmons LW, Emlen DJ. Evolutionary trade-off between weapons and testes. Proceedings of the National Academy of Sciences of the United States of America. 2006;103:16346–16351. doi: 10.1073/pnas.0603474103. PubMed DOI PMC

Simmons LW, Fitzpatrick JL. Sperm wars and the evolution of male fertility. Reproduction. 2012;144:519–534. doi: 10.1530/REP-12-0285. PubMed DOI

Simpson JL, Humphries S, Evans JP, Simmons LW, Fitzpatrick JL. Relationships between sperm length and speed differ among three internally and three externally fertilizing species. Evolution. 2014;68:92–104. doi: 10.1111/evo.12199. PubMed DOI

Soler AJ, Garde JJ. Relationship between the characteristics of epididymal red deer spermatozoa and penetrability into zona-free hamster ova. Journal of Andrology. 2003;24:393–400. PubMed

Stopher KV, Nussey DH, Clutton-Brock TH, Guinness F, Morris A, Pemberton JM. The red deer rut revisited: female excursions but no evidence females move to mate with preferred males. Behavioral Ecology. 2011;22:808–818. doi: 10.1093/beheco/arr052. DOI

Turner RM. Moving to the beat: a review of mammalian sperm motility regulation. Reproduction, Fertility, and Development. 2006;18:25–38. doi: 10.1071/RD05120. PubMed DOI

Van der Horst G, Maree L. Sperm form and function in the absence of sperm competition. Molecular Reproduction and Development. 2014;81:204–216. doi: 10.1002/mrd.22277. PubMed DOI

Varea-Sánchez M, Gómez Montoto L, Tourmente M, Roldan ERS. Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents. PLoS ONE. 2014;9:e1478. doi: 10.1371/journal.pone.0108148. PubMed DOI PMC

Horn size is linked to Sertoli cell efficiency and sperm size homogeneity during sexual development in common eland (Taurotragus oryx)

Spermatogenic Activity and Sperm Traits in Post-Pubertal and Adult Tomcats (Felis catus): Implication of Intra-Male Variation in Sperm Size

High-energy diet enhances spermatogenic function and increases sperm midpiece length in fallow deer (Dama dama) yearlings

Current status and potential of morphometric sperm analysis