Delineating the roles of males and females in sperm competition

Proceedings of the Royal Society B: Biological Sciences

Volumn 280, Issue 1772, 2013, Pages

  Evans, Jonathan P ^a   Rosengrave, Patrice ^b   Gasparini, Clelia ^a   Gemmell, Neil J ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Cryptic female choice; Genetic compatibility; Interacting phenotypes; Multiple mating; Polyandry

Indexed keywords

COMPETITIVE ABILITY; CRYPSIS; MATE CHOICE; PATERNITY; POLYANDRY; REPRODUCTIVE SUCCESS; SALMONID; SEX ROLE; SEXUAL SELECTION; SPERM COMPETITION;

ANIMAL; ARTICLE; FEMALE; FERTILIZATION; GENETIC VARIABILITY; MALE; NEW ZEALAND; ONCORHYNCHUS; PHYSIOLOGY; SPERMATOZOON;

ANIMALS; FEMALE; FERTILIZATION; GENETIC VARIATION; MALE; NEW ZEALAND; ONCORHYNCHUS; PHYSIOLOGY; SPERMATOZOA;

EID: 84902658121     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2047     Document Type: Article

References (54)

1. Birkhead TR, Møller AP. 1998 Sperm competition and sexual selection. San Diego, CA: Academic Press.
2. Simmons LW, Fitzpatrick JL. 2012 Sperm wars and the evolution of male fertility. Reproduction 144, 519-534. (doi:10.1530/REP-12-0285)
3. Pizzari T, Parker GA. 2009 Sperm competition and sperm phenotype. In Sperm biology: an evolutionary perspective (eds TR Birkhead, DJ Hosken, S Pitnick), pp. 207-245. Burlington, MA: Academic Press.
4. Karr TL, Swanson WJ, Snook RR. 2009 The evolutionary significance of variation in sperm-egg interactions. In Sperm biology: an evolutionary perspective (eds TR Birkhead, DJ Hosken, S Pitnick), pp. 305-365. Burlington, MA: Academic Press.
5. Thornhill R. 1983 Cryptic female choice and its implications in the scorpionfly Harpobittacus nigricepts. Am. Nat. 122, 765-788. (doi:10.1086/ 284170)
6. Gillingham MAF, Richardson DS, Lovlie H, Moynihan A, Worley K, Pizzari T. 2009 Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus. Proc. R. Soc. B 276, 1083-1092. (doi:10.1098/rspb.2008.1549)
7. Bretman A, Newcombe D, Tregenza T. 2009 Promiscuous females avoid inbreeding by controlling sperm storage. Mol. Ecol. 18, 3340-3345. (doi:10.1111/j.1365-294X.2009.04301.x)
8. Gasparini C, Pilastro A. 2011 Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. R. Soc. B 278, 2495-2501. (doi:10.1098/ rspb.2008.1549)
9. Evans JP, Rutstein AN. 2008 Postcopulatory sexual selection favours intrinsically good sperm competitors. Behav. Ecol. Sociobiol. 62, 1167-1173. (doi:10.1007/s00265-008-0545-0)
10. Radwan J. 1998 Heritability of sperm competition success in the bulb mite, Rhizoglyphus robini. J. Evol. Biol. 11, 321-327.
11. Tregenza T, Attia F, Bushaiba SS. 2009 Repeatability and heritability of sperm competition outcomes in males and females of Tribolium castaneum. Behav. Ecol. Sociobiol. 63, 817-823. (doi:10.1007/s00265-009-0716-7)
12. Edvardsson M, Arnqvist G. 2000 Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum. Proc. R. Soc. Lond. B 267, 559-563. (doi:10.1098/rspb.2000.1037)
13. Clark AG, Begun DJ, Prout T. 1999 Female x male interactions in Drosophila sperm competition. Science 283, 217-220. (doi:10.1126/science.283.5399.217)
14. Zhang R, Clark AG, Fiumera AC. 2013 Natural genetic variation in male reproductive genes contributes to nontransitivity of sperm competitive ability in Drosophila melanogaster. Mol. Ecol. 22, 1400-1415. (doi:10.1111/mec.12113)
15. Bjork A, Starmer WT, Higginson DM, Rhodes CJ, Pitnick S. 2007 Complex interactions with females and rival males limit the evolution of sperm offence and defence. Proc. R. Soc. B 274, 1779-1788. (doi:10.1098/rspb.2007.0293)
16. Engqvist L. 2013 A general description of additive and nonadditive elements of sperm competitiveness and their relation to male fertilization success. Evolution 67, 1396-1405.
17. Garcia-Gonzalez F, Evans JP. 2011 Fertilization success and the estimation of genetic variance in sperm competitiveness. Evolution 65, 746-756. (doi:10.1111/j.1558-5646.2010.01127.x)
18. García-González F. 2008 The relative nature of fertilization success: implications for the study of post-copulatory sexual selection. BMC Evol. Biol. 8, 140. (doi:10.1186/1471-2148-8-140)
19. Bentzen P, Olsen JB, McLean JE, Seamons TR, Quinn TP. 2001 Kinship analysis of Pacific salmon: insights into mating, homing, and timing of reproduction. J. Hered. 92, 127-136. (doi:10.1093/jhered/92.2.127)
20. Turner E, Montgomerie R. 2002 Ovarian fluid enhances sperm movement in Arctic charr. J. Fish Biol. 60, 1570-1579. (doi:10.1111/j.1095-8649.2002.tb02449.x)
21. Butts IAE, Johnson K, Wilson CC, Pitcher TE. 2012 Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush. Theriogenology 78, 2105-2109. (doi:10.1016/j. theriogenology.2012.06.031)
22. Dietrich GJ, Wojtczak M, Slowinska M, Dobosz S, Kuzminski H, Ciereszko A. 2008 Effects of ovarian fluid on motility characteristics of rainbow trout (Oncorhynchus mykiss Walbaum) spermatozoa. J. Appl. Ichthyol. 24, 503-507. (doi:10.1111/j.1439-0426.2006.01130.x)
23. Rosengrave R, Gemmell NJ, Metcalf V, McBride K, Montgomerie R. 2008 A mechanism for cryptic female choice in chinook salmon. Behav. Ecol. 19, 1179-1185. (doi:10.1093/beheco/arn089)
24. Urbach D, Folstad I, Rudolfsen G. 2005 Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus). Behav. Ecol. Sociobiol. 57, 438-444. (doi:10.1007/s00265-004-0876-4)
25. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA. 2004 Spermatozoal traits and sperm competition in Atlantic salmon: relative velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44-47.
26. Unwin MJ, Quinn TP, Kinnison MT, Boustead NC. 2000 Divergence in juvenile growth and life history in two recently colonized and partially isolated chinook salmon populations. J. Fish Biol. 57, 943-960. (doi:10.1111/j.1095-8649.2000. tb02203.x)
27. Walsh PS, Metzger DA, Higuchi R. 1991 Chelex-100 as a medium for simple extraction of DNA for PCRbased typing from forensic material. Biotechniques 10, 506-513.
28. Condrey MJ, Bentzen P. 1998 Characterization of coastal cutthroat trout (Oncorhynchus clarki clarki) microsatellites and their conservation in other salmonids. Mol. Ecol. 7, 787-789.
29. Beacham TD, Candy JR, Le KD, Wetklo M. 2009 Population structure of chum salmon (Oncorhynchus keta) across the Pacific Rim, determined from microsatellite analysis. Fish. Bull. 107, 244-260.
30. Banks MA, Blouin MS, Baldwin BA, Rashbrook VK, Fitzgerald HA, Blankenship SM, Hedgecock D. 1999 Isolation and inheritance of novel microsatellites in chinook salmon (Oncorhynchus tschawytscha). J. Hered. 90, 281-288. (doi:10.1093/jhered/90.2.281)
31. Heath DD, Bryden CA, Shrimpton JM, Iwama GK, Kelly J, Heath JW. 2002 Relationships between heterozygosity, allelic distance (d2), and reproductive traits in chinook salmon, Oncorhynchus tshawytscha. Can. J. Fish. Aquat. Sci. 59, 77-84. (doi:10.1139/f01-192)
32. Kalinowski ST, Taper ML, Marshall TC. 2007 Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099-1106. (doi:10. 1111/j.1365-294X.2007.03089.x)
33. Queller DC, Goodnight KF. 1989 Estimating relatedness using genetic markers. Evolution 43, 258-275. (doi:10.2307/2409206)
34. Wang J. 2011 COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Res. 11, 141-145. (doi:10.1111/j.1755-0998.2010.02885.x)
35. Nakagawa S, Schielzeth H. 2010 Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935-956.
36. R Development Core Team. 2011 A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
37. Bates D, Maechler M, Dai B. 2008 lme4: linear mixed-effects models using S4 classes. R package version 0.999375-37. See http://lme4.r-forge.rproject. org.
38. 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. (doi:10.1016/j.tree.2008.10.008)
39. Blukacz EA et al. 2010 Linking lake whitefish (Coregonus clupeaformis) condition with male gamete quality and quantity. J. Gt. Lakes Res. 36, 78-83. (doi:10.1016/j.jglr.2009.12.014)
40. Browne WJ, Subramanian SV, Jones K, Goldstein H. 2005 Variance partitioning in multilevel logistic models that exhibit overdispersion. J. R. Stat. Soc. A 168, 599-613. (doi:10.1111/j.1467-985X.2004.00365.x)
41. Evans JP, Garcia-Gonzalez F, Almbro M, Robinson O, Fitzpatrick JL. 2012 Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate. Proc. R. Soc. B 279, 2855-2861. (doi:10.1098/rspb.2012.0181)
42. Hood GM. 2009 PopTools version 3.1.1. See http:// www.cse.csiro.au/poptools.
43. Galvano PM, Johnson K, Wilson CC, Pitcher TE, Butts IAE. 2013 Ovarian fluid influences sperm performance in lake trout, Salvelinus namaycush. Reprod. Biol. 13, 172-175. (doi:10.1016/j.repbio.2013.02.001)
44. Elofsson H, Van Look KJW, Sundell K, Sundh H, Borg B. 2006 Stickleback sperm saved by salt in ovarian fluid. J. Exp. Biol. 209, 4230-4237. (doi:10.1242/ jeb.02481)
45. Yeates SE, Diamond SE, Einum S, Emerson BC, Holt WV, Gage MJG. In press. Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior. Evolution (doi:10.1111/evo.12208)
46. Parker GA. 1990 Sperm competition games: raffles and roles. Proc. R. Soc. Lond. B 242, 120-126. (doi:10.1098/rspb.1990.0114)
47. Engqvist L. 2012 Genetic conflicts, intrinsic male fertility, and ejaculate investment. Evolution 66, 2685-2696. (doi:10.1111/j.1558-5646.2012.01641.x)
48. Olsson M, Pagel M, Shine R, Madsen T. 1999 Sperm choice and sperm competition: suggestions for field and laboratory studies. Oikos 84, 172-175. (doi:10. 2307/3546880)
49. Droge-Young EM, Manier MK, Lupold S, Belote JM, Pitnick S. 2012 Covariance among premating, postcopulatory and viability fitness components in Drosophila melanogaster and their influence on paternity measurement. J. Evol. Biol. 25, 1555-1563. (doi:10.1111/j.1420-9101.2012.02540.x)
50. García-González F. 2008 Male genetic quality and the inequality between paternity success and fertilization success: consequences for studies of sperm competition and the evolution of polyandry. Evolution 62, 1653-1665. (doi:10.1111/j.1558-5646.2008.00362.x)
51. Gilchrist AS, Partridge L. 1997 Heritability of preadult viability differences can explain apparent heritability of sperm displacement ability in Drosophila melanogaster. Proc. R. Soc. Lond. B 264, 1271-1275. (doi:10.1098/rspb.1997.0175)
52. Yasui Y. 1997 A 'good-sperm' model can explain the evolution of costly multiple mating by females. Am. Nat. 149, 573-584. (doi:10.1086/286006)
53. Evans JP, Simmons LW. 2008 The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good-and sexy-sperm? Genetica 134, 5-19. (doi:10.1007/ s10709-007-9162-5)
54. Fricke C, Martin OY, Bretman A, Bussiere LF, Chapman T. 2010 Sperm competitive ability and indices of lifetime reproductive success. Evolution 64, 2746-2757. (doi:10.1111/j.1558-5646.2010.01022.x)