Sperm form and function: what do we know about the role of sexual selection?

in Reproduction

Sperm morphological variation has attracted considerable interest and generated a wealth of predominantly descriptive studies over the past three centuries. Yet, apart from biophysical studies linking sperm morphology to swimming velocity, surprisingly little is known about the adaptive significance of sperm form and the selective processes underlying its tremendous diversification throughout the animal kingdom. Here, we first discuss the challenges of examining sperm morphology in an evolutionary context and why our understanding of it is far from complete. Then, we review empirical evidence for how sexual selection theory applies to the evolution of sperm form and function, including putative secondary sexual traits borne by sperm.

 

    Society for Reproduction and Fertility

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    Sperm morphological diversity. Scanning electron micrographs of (A) Macrobiotus cf. hufelandi (Tardigrada: Macrobiotidae; L. Rebecchi, U. of Modena e Reggio Emilia), (B) Caenorhabditis elegans (Nematoda: Rhabditida; T Roberts, Florida State University, FL, USA), (C) Mytilocypris mytiloides (Crustacea: Ostracoda – posterior end of long, filiform sperm; R Matzke-Karasz, Ludwig Maximilian University, Munich, germany), (D) Drosophila bifurca (Insecta: Drosophilidae; R Dallai, University of Siena), (E) Patinopecten yessoensis (Mollusca: Ostreoida; from Li et al. 2000), (F) Iporangaia pustulosa (Arachnida: Opiliones; from Moya et al. 2007), (G) Trialeurodes vaporariorum (Insecta: Aleyrodidae; R Dallai), (H) Allacma fusca (Hexapoda: Sminthuridae; from Dallai et al. 2009), (I) Colostethus marchesianus (Anura: Aromobatidae; from Veiga-Menoncello et al. 2007), (J) Paralichthys olivaceus (Actinopterygii: Paralichthyidae; from Zhang et al. 2003), (K) Gopherus agassizii (Reptilia: Testudinata; L Liaw, Beckman Laser Institute at University of California Irvine, CA, USA), (L) Passer domesticus (Aves: Passeridae; R Dallai), (M) Phataginus tricuspi (Pholidota: Manidae; L Liaw), (N) Uromys caudimaculatus (Rodentia: Muridae; W Breed, University of Adelaide, Australia). All published photos reprinted with permission from Elsevier; all unpublished photos courtesy of authors in parentheses.

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    Variation in sperm length across the animal kingdom (in µm on a logarithmic scale). Each horizontal line spans the range of sperm lengths reported in the literature for each taxon. Line colors depict different fertilization modes (light gray: external fertilization, from broadcast spawning in marine invertebrates to female-directed sperm release in frogs; dark gray: spermcasting; black: internal fertilization). Dotted lines indicate considerable extension of the sperm length range by inclusion of an extreme outlier (e.g., Neoceratodus forsteri in the externally fertilizing bony fishes and Discoglossus pictus in the frogs). Data were retrieved from Pitnick et al. (2009a), with an extended range for seed shrimp based on Wingstrand (1988) and Smith et al. (2016).

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    Schematic illustration of a likely process of postcopulatory sexual selection on sperm length in Drosophila, involving aspects of both sperm competition and cryptic female choice. SS, sexual selection at both pre- and postmating stages.

References

AfzeliusBA 1995 Gustaf Retzius and spermatology. International Journal of Developmental Biology 39 675685.

Ah-KingMBarronABHerbersteinME 2014 Genital evolution: why are females still understudied? PLoS Biology 12 17. (https://doi.org/10.1371/journal.pbio.1001851)

AlbertiG 1990 Comparative spermatology of Araneae. Acta Zoologica Fennica 190 1734.

AllenBJLevintonJS 2007 Costs of bearing a sexually selected ornamental weapon in a fiddler crab. Functional Ecology 21 154161.

AlonzoSHStiverKAMarsh-RolloSE 2016 Ovarian fluid allows directional cryptic female choice despite external fertilization. Nature Communications 7 12452. (https://doi.org/10.1038/ncomms12452)

AlvarezL 2017 The tailored sperm cell. Journal of Plant Research 130 455464. (https://doi.org/10.1007/s10265-017-0936-2)

AnderssonM 1994 Sexual Selection. Princeton, New Jersey: Princeton University Press.

ArnqvistGRoweL 2005 Sexual Conflict. Princeton, NJ: Princeton University Press.

AvilaFWSirotLKLaFlammeBARubinsteinCDWolfnerMF 2011 Insect seminal fluid proteins: identification and function. Annual Review of Entomology 56 2140. (https://doi.org/10.1146/annurev-ento-120709-144823)

BallMAParkerGA 2003 Sperm competition games: sperm selection by females. Journal of Theoretical Biology 224 2742. (https://doi.org/10.1016/S0022-5193(03)00118-8)

BalshineSLeachBJNeatFWernerNYMontgomerieR 2001 Sperm size of African cichlids in relation to sperm competition. Behavioral Ecology 12 726731. (https://doi.org/10.1093/beheco/12.6.726)

BennisonCHemmingsNSlateJBirkheadTBennisonC 2015 Long sperm fertilize more eggs in a bird. Proceedings of the Royal Society B 282 20141897. (https://doi.org/10.1098/rspb.2014.1897)

BerglundABisazzaAPilastroA 1996 Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biological Journal of the Linnean Society 58 385399. (https://doi.org/10.1111/j.1095-8312.1996.tb01442.x)

BianchiEWrightGJ 2016 Sperm meets egg: the genetics of mammalian fertilization. Annual Review of Genetics 50 93111. (https://doi.org/10.1146/annurev-genet-121415-121834)

BirkheadTR 1998 Cryptic female choice: criteria for establishing female sperm choice. Evolution 52 12121218. (https://doi.org/10.1111/j.1558-5646.1998.tb01848.x)

BirkheadTRBigginsJD 1998 Sperm competition mechanisms in birds: models and data. Behavioral Ecology 9 253260. (https://doi.org/10.1093/beheco/9.3.253)

BirkheadTRHunterFM 1990 Mechanisms of sperm competition. Trends in Ecology and Evolution 5 4852. (https://doi.org/10.1016/0169-5347(90)90047-H)

BirkheadTRMøllerAP 1993 Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biological Journal of the Linnean Society 50 295311. (https://doi.org/10.1111/j.1095-8312.1993.tb00933.x)

BirkheadTRMonaghanP 2010 Ingenious ideas: the history of behavioral ecology. In Evolutionary Behavioral Ecology pp 315. Eds WestneatDF & FoxCW. New York: Oxford University Press.

BirkheadTRMontgomerieR 2009 Three centuries of sperm research. In Sperm Biology: An Evolutionary Perspective pp 142. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

BirkheadTRPellattEJFletcherF 1993a Selection and utilization of spermatozoa in the reproductive tract of the female zebra finch Taeniopygia guttata. Journal of Reproduction and Fertility 99 593600. (https://doi.org/10.1530/jrf.0.0990593)

BirkheadTRMøllerAPSutherlandWJ 1993b Why do females make it so difficult for males to fertilize their eggs? Journal of Theoretical Biology 161 5160. (https://doi.org/10.1006/jtbi.1993.1039)

BirkheadTRChalineNBigginsJDBurkeTPizzariT 2004 Nontransitivity of paternity in a bird. Evolution 58 416420. (https://doi.org/10.1111/j.0014-3820.2004.tb01656.x)

BirkheadTRPellattEJBrekkePYeatesRCastillo-JuarezH 2005 Genetic effects on sperm design in the zebra finch. Nature 434 383387. (https://doi.org/10.1038/nature03374)

BjorkAPitnickS 2006 Intensity of sexual selection along the anisogamy-isogamy continuum. Nature 441 742745. (https://doi.org/10.1038/nature04683)

BjorkAStarmerWTHigginsonDMRhodesCJPitnickS 2007 Complex interactions with females and rival males limit the evolution of sperm offence and defence. Proceedings of the Royal Society B 274 17791788. (https://doi.org/10.1098/rspb.2007.0293)

BriskieJVMontgomerieR 1992 Sperm size and sperm competition in birds. Proceedings of the Royal Society B 247 8995. (https://doi.org/10.1098/rspb.1992.0013)

BriskieJVMontgomerieRBirkheadTR 1997 The evolution of sperm size in birds. Evolution 51 937945. (https://doi.org/10.1111/j.1558-5646.1997.tb03674.x)

ByrnePGSimmonsLWRobertsJD 2003 Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society B 270 20792086. (https://doi.org/10.1098/rspb.2003.2433)

CivettaA 1999 Direct visualization of sperm competition and sperm storage in Drosophila. Current Biology 9 841844. (https://doi.org/10.1016/S0960-9822(99)80370-4)

ClarkAGBegunDJProutT 1999 Female × male interactions in Drosophila sperm competition. Science 389 217220. (https://doi.org/10.1126/science.283.5399.217)

CottonSFowlerKPomiankowskiA 2004 Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proceedings of the Royal Society B 271 771783. (https://doi.org/10.1098/rspb.2004.2688)

CurtsingerJW 1991 Sperm competition and the evolution of multiple mating. American Naturalist 138 93102. (https://doi.org/10.1086/285206)

DallaiR 1979 An overview of atypical spermatozoa in insects. In The Spermatozoon pp 253265. Eds FawcettDW & BedfordJM. Baltimore: Urban and Schwarzenberg.

DallaiRLupettiPMencarelliC 2006 Unusual axonemes of hexapod spermatozoa. International Review of Cytology 254 4599. (https://doi.org/10.1016/S0074-7696(06)54002-1)

DallaiRZizzariZVFanciulliPP 2009 Different sperm number in the spermatophores of Orchesella villosa (Geoffroy) (Entomobryidae) and Allacma fusca (L.) (Sminthuridae). Arthropod Structure & Development 38 227234. (https://doi.org/10.1016/j.asd.2008.10.002)

DarwinC 1871 The Descent of Man and Selection in Relation to Sex. London: John Murray.

DewsburyDA 1982 Ejaculate cost and male choice. American Naturalist 119 601610. (https://doi.org/10.1086/283938)

DorusSKarrTL 2009 Sperm proteomics and genomics. In Sperm Biology: An Evolutionary Perspective pp 435469. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

Droge-YoungEMBeloteJMPerezGSPitnickS 2016 Resolving mechanisms of short-term competitive fertilization success in the red flour beetle. Journal of Insect Physiology 93–94 110. (https://doi.org/10.1016/j.jinsphys.2016.06.003)

DybasLKDybasHS 1981 Coadaptation and taxonomic differentiation of sperm and spermathecae in featherwing beetles. Evolution 35 168174. (https://doi.org/10.1111/j.1558-5646.1981.tb04869.x)

EberhardWG 1996 Female Control: Sexual Selection by Cryptic Female Choice. Princeton, New Jersey: Princeton University Press.

EberhardWG 2000 Criteria for demonstrating postcopulatory female choice. Evolution 54 10471050. (https://doi.org/10.1111/j.0014-3820.2000.tb00105.x)

EmlenDJ 2001 Costs and the diversification of exaggerated animal structures. Science 291 15341536. (https://doi.org/10.1126/science.1056607)

EvansJPMarshallDJ 2005 Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59 106112. (https://doi.org/10.1111/j.0014-3820.2005.tb00898.x)

EvansJPShermanCDH 2013 Sexual selection and the evolution of egg-sperm interactions in broadcast-spawning invertebrates. Biological Bulletin 224 166183. (https://doi.org/10.1086/BBLv224n3p166)

FindlayGDSitnikJLWangWAquadroCFClarkNLWolfnerMF 2014 Evolutionary rate covariation identifies new members of a protein network required for Drosophila melanogaster female post-mating responses. PLoS Genetics 10 e1004108. (https://doi.org/10.1371/journal.pgen.1004108)

FirmanRCGaspariniCManierMKPizzariT 2017 Postmating female control: 20 years of cryptic female choice. Trends in Ecology and Evolution 32 368382. (https://doi.org/10.1016/j.tree.2017.02.010)

FitzpatrickJLLüpoldS 2014 Sexual selection and the evolution of sperm quality. Molecular Human Reproduction 20 11801189. (https://doi.org/10.1093/molehr/gau067)

FitzpatrickJLMontgomerieRDesjardinsJKStiverKAKolmNBalshineS 2009 Female promiscuity promotes the evolution of faster sperm in cichlid fishes. PNAS 106 11281132. (https://doi.org/10.1073/pnas.0809990106)

FujinokiMTakeiGLKonH 2016 Non-genomic regulation and disruption of spermatozoal in vitro hyperactivation by oviductal hormones. Journal of Physiological Sciences 66 207212. (https://doi.org/10.1007/s12576-015-0419-y)

GageMJG 1994 Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society B 258 247254. (https://doi.org/10.1098/rspb.1994.0169)

GageMJGCookPA 1994 Sperm size or numbers? Effects of nutritional stress upon eupyrene and apyrene sperm production strategies in the moth Plodia interpunctella (Lepidoptera: Pyralidae). Functional Ecology 8 594599. (https://doi.org/10.2307/2389920)

GilbertSFBarresiMJ 2016 Developmental Biology. Sunderland, MA: Sinauer Associates.

GomendioMRoldanERS 1993 Mechanisms of sperm competition: linking physiology and behavioural ecology. Trends in Ecology and Evolution 8 95100. (https://doi.org/10.1016/0169-5347(93)90059-X)

GomendioMRoldanERS 2008 Implications of diversity in sperm size and function for sperm competition and fertility. International Journal of Developmental Biology 52 439447. (https://doi.org/10.1387/ijdb.082595mg)

GrafenA 1990 Sexual selection unhandicapped by the Fisher process. Journal of Theoretical Biology 144 517546. (https://doi.org/10.1016/S0022-5193(05)80088-8)

HellriegelBBernasconiG 2000 Female-mediated differential sperm storage in a fly with complex spermathecae, Scatophaga stercoraria. Animal Behaviour 59 311317. (https://doi.org/10.1006/anbe.1999.1308)

HellriegelBWardPI 1998 Complex female reproductive tract morphology: its possible use in postcopulatory female choice. Journal of Theoretical Biology 190 179186. (https://doi.org/10.1006/jtbi.1997.0546)

HigginsonDMPitnickS 2011 Evolution of intra-ejaculate sperm interactions: do sperm cooperate? Biological Reviews 86 249270. (https://doi.org/10.1111/j.1469-185X.2010.00147.x)

HigginsonDMMillerKBSegravesKAPitnickS 2012 Female reproductive tract form drives the evolution of complex sperm morphology. PNAS 109 45384543. (https://doi.org/10.1073/pnas.1111474109)

HillGE 2011 Condition-dependent traits as signals of the functionality of vital cellular processes. Ecology Letters 14 625634. (https://doi.org/10.1111/j.1461-0248.2011.01622.x)

WVHoltFazeliA 2016 Sperm selection in the female mammalian reproductive tract. Focus on the oviduct: hypotheses, mechanisms, and new opportunities. Theriogenology 85 105112. (https://doi.org/10.1016/j.theriogenology.2015.07.019)

HotzyCPolakMRönnJLArnqvistG 2012 Phenotypic engineering unveils the function of genital morphology. Current Biology 22 22582261. (https://doi.org/10.1016/j.cub.2012.10.009)

HouleD 1998 How should we explain variation in the genetic variance of traits? Genetica 102/103 241253. (https://doi.org/10.1023/A:1017034925212)

HuntJBreukerCJSadowskiJAMooreAJ 2009 Male-male competition, female mate choice and their interaction: determining total sexual selection. Journal of Evolutionary Biology 22 1326. (https://doi.org/10.1111/j.1420-9101.2008.01633.x)

ImmlerSSaint-JalmeMLesobreLSorciGRomanYBirkheadTR 2007 The evolution of sperm morphometry in pheasants. Journal of Evolutionary Biology 20 10081014. (https://doi.org/10.1111/j.1420-9101.2007.01302.x)

ImmlerSPitnickSParkerGADurrantKLLüpoldSCalhimSBirkheadTR 2011 Resolving variation in the reproductive tradeoff between sperm size and number. PNAS 108 53255330. (https://doi.org/10.1073/pnas.1009059108)

IwasaYPomiankowskiANeeS 1991 The evolution of costly mate preferences. II. The handicap principle. Evolution 45 14311442. (https://doi.org/10.1111/j.1558-5646.1991.tb02646.x)

JamiesonBGM 1987 The Ultrastructure and Phylogeny of Insect Spermatozoa. Cambridge: Cambridge University Press.

JamiesonBGM 1991 Fish Evolution and Systematics: Evidence from Spermatozoa. Cambridge: Cambridge University Press.

JennionsMDPetrieM 1997 Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews 72 283327. (https://doi.org/10.1017/S0006323196005014)

KahrlAFCoxRM 2015 Diet affects ejaculate traits in a lizard with condition-dependent fertilization success. Behavioral Biology 26 15021511. (https://doi.org/10.1093/beheco/arv105)

KaldunBOttiO 2016 Condition-dependent ejaculate production affects male mating behavior in the common bedbug Cimex lectularius. Ecology and Evolution 6 25482558. (https://doi.org/10.1002/ece3.2073)

KarrTLSwansonWJSnookRR 2009 The evolutionary significance of variation in sperm–egg interactions. In Sperm Biology: An Evolutionary Perspective pp 305365. San Diego: Academic Press.

KatzDF 1983 The evolution of mammalian sperm motility in the male and female reproductive. In The Sperm Cell pp 340344. Ed AndréJ The Hague: Marinus Nijhoff Publishers.

KatzDF 1991 Characteristics of sperm motility. Annals of the New York Academy of Sciences 637 409423. (https://doi.org/10.1111/j.1749-6632.1991.tb27326.x)

KellerLReeveHK 1995 Why do females mate with multiple males? The sexually selected sperm hypothesis. Advances in the Study of Behavior 24 291315.

KimK-WBennisonCHemmingsNBrookesLHurleyLLGriffithSCBurkeTBirkheadTRSlateJ 2017 A sex-linked supergene controls sperm morphology and swimming speed in a songbird. Nature Ecology and Evolution 1 11681176. (https://doi.org/10.1038/s41559-017-0235-2)

KingLMBrillardJPGarrettWMBakstMRDonoghueAM 2002 Segregation of spermatozoa within sperm storage tubules of fowl and turkey hens. Reproduction 123 7986. (https://doi.org/10.1530/rep.0.1230079)

KirkpatrickMRyanMJ 1991 The evolution of mating preferences and the paradox of the lek. Nature 350 3338. (https://doi.org/10.1038/350033a0)

KirkpatrickMRandASRyanMJ 2006 Mate choice rules in animals. Animal Behaviour 71 12151225. (https://doi.org/10.1016/j.anbehav.2005.11.010)

KlevenOFossøyFLaskemoenTRobertsonRJRudolfsenGLifjeldJT 2009 Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63 24662473. (https://doi.org/10.1111/j.1558-5646.2009.00725.x)

LaMunyonCWWardS 1998 Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proceedings of the Royal Society B 265 19972002. (https://doi.org/10.1098/rspb.1998.0531)

LaMunyonCWWardS 1999 Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proceedings of the Royal Society B 266 263267. (https://doi.org/10.1098/rspb.1999.0631)

LandeR 1980 Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34 292305. (https://doi.org/10.1111/j.1558-5646.1980.tb04817.x)

LeonardJLCórdoba-AguilarA 2010 The Evolution of Primary Sexual Characters in Animals. Princeton, NJ: Oxford University Press.

LessellsCMBirkheadTR 1990 Mechanisms of sperm competition in birds: mathematical models. Behavioral Ecology and Sociobiology 27 325337. (https://doi.org/10.1007/BF00164003)

LewisSMAustadSN 1990 Sources of intraspecific variation in sperm precedence in red flour beetles. American Naturalist 135 351359. (https://doi.org/10.1086/285050)

LiQOsadaMKashiharaMHirohashiKKijimaA 2000 Effects of ultraviolet irradiation on genetical inactivation and morphological structure of sperm of the Japanese scallop, Patinopecten yessoensis. Aquaculture 186 233242. (https://doi.org/10.1016/S0093-691X(03)00097-9)

LiaoWBHuangYZengYZhongMJLuoYLüpoldS 2018 Ejaculate evolution in external fertilizers: influenced by sperm competition or sperm limitation? Evolution 72 417. (https://doi.org/10.1111/evo.13372)

LüpoldSFitzpatrickJL 2015 Sperm number trumps sperm size in mammalian ejaculate evolution. Proceedings of the Royal Society B 282 20152122. (https://doi.org/10.1098/rspb.2015.2122)

LüpoldSCalhimSImmlerSBirkheadTR 2009a Sperm morphology and sperm velocity in passerine birds. Proceedings of the Royal Society B 276 11751181. (https://doi.org/10.1098/rspb.2008.1645)

LüpoldSLinzGMBirkheadTR 2009b Sperm design and variation in the New World blackbirds (Icteridae). Behavioral Ecology and Sociobiology 63 899909. (https://doi.org/10.1007/s00265-009-0733-6)

LüpoldSLinzGMRiversJWWestneatDFBirkheadTR 2009c Sperm competition selects beyond relative testes size in birds. Evolution 63 391402. (https://doi.org/10.1111/j.1558-5646.2008.00571.x)

LüpoldSManierMKBerbenKSSmithKJDaleyBDBuckleySHBeloteJMPitnickS 2012 How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Current Biology 22 16671672. (https://doi.org/10.1016/j.cub.2012.06.059)

LüpoldSPitnickSBerbenKSBlenginiCSBeloteJMManierMK 2013 Female mediation of competitive fertilization success in Drosophila melanogaster. PNAS 110 1069310698. (https://doi.org/10.1073/pnas.1300954110)

LüpoldSManierMKPuniamoorthyNSchoffCStarmerWTLuepoldSHBBeloteJMPitnickS 2016 How sexual selection can drive the evolution of costly sperm ornamentation. Nature 533 535538. (https://doi.org/10.1038/nature18005)

LymberyRAKenningtonWJEvansJP 2016 Fluorescent sperm offer a method for tracking the real-time success of ejaculates when they compete to fertilise eggs. Scientific Reports 6 18. (https://doi.org/10.1038/s41598-016-0001-8)

ManierMKBeloteJMBerbenKSNovikovDStuartWTPitnickS 2010 Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328 354357. (https://doi.org/10.1126/science.1187096)

ManierMKBeloteJMBerbenKSLüpoldSAla-HonkolaOCollinsWFPitnickS 2013a Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67 23482362. (https://doi.org/10.1111/evo.12117)

ManierMKLüpoldSBeloteJMStarmerWTBerbenKSAla-HonkolaOCollinsWFPitnickS 2013b Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Current Biology 23 18531862. (https://doi.org/10.1016/j.cub.2013.07.086)

Marie-OrleachLJanickeTVizosoDBEichmannMSchärerL 2014 Fluorescent sperm in a transparent worm: validation of a GFP marker to study sexual selection. BMC Evolutionary Biology 14 148. (https://doi.org/10.1186/1471-2148-14-148)

MartinPAReimersTJLodgeJRDziukPJ 1974 Effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. Journal of Reproduction and Fertility 39 251258. (https://doi.org/10.1530/jrf.0.0390251)

MautzBSMøllerAPJennionsMD 2013 Do male secondary sexual characters signal ejaculate quality? A meta-analysis. Biological Reviews 88 669682. (https://doi.org/10.1111/brv.12022)

McLeodDVDayT 2017 Female plasticity tends to reduce sexual conflict. Nature Ecology and Evolution 1 54. (https://doi.org/10.1038/s41559-016-0054)

MillerGTPitnickS 2002 Sperm-female coevolution in Drosophila. Science 298 12301233. (https://doi.org/10.1126/science.1076968)

MillerGTPitnickS 2003 Functional significance of seminal receptacle length in Drosophila melanogaster. Journal of Evolutionary Biology 16 114126. (https://doi.org/10.1046/j.1420-9101.2003.00476.x)

MinderAMHoskenDJWardPI 2005 Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). Journal of Evolutionary Biology 18 6069. (https://doi.org/10.1111/j.1420-9101.2004.00799.x)

MorrowEHGageMJG 2000 The evolution of sperm length in moths. Proceedings of the Royal Society B 267 307313. (https://doi.org/10.1098/rspb.2000.1001)

MoyaJManciniKMachadoGDolderH 2007 Sperm morphology of the neotropical harvestman Iporangaia pustulosa (Arachnida: Opiliones): Comparative morphology and functional aspects. Arthropod Structure & Development 36 5362. (https://doi.org/10.1016/j.asd.2006.07.006)

NilssonTFrickeCArnqvistG 2003 The effects of male and female genotype on variance in male fertilization success in the red flour beetle (Tribolium castaneum). Behavioral Ecology and Sociobiology 53 227233. (https://doi.org/10.1007/s00265-002-0565-0)

OliverJHJ 1982 Tick reproduction: sperm development and cytogenetics. In Physiology of Ticks pp 245275. Eds ObenchainFD & GalunR. Oxford: Pergamon Press.

OlssonMMadsenTShineR 1997 Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proceedings of the Royal Society B 264 455459. (https://doi.org/10.1098/rspb.1997.0065)

OrrTJBrennanPLR 2015 Sperm storage: distinguishing selective processes and evaluating criteria. Trends in Ecology and Evolution 30 261272. (https://doi.org/10.1016/j.tree.2015.03.006)

ParkerGA 1970 Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45 526567.

ParkerGA 1979 Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects pp 123166. Eds BlumMS & BlumNA. New York: Academic Press.

ParkerGA 1982 Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. Journal of Theoretical Biology 96 281294. (https://doi.org/10.1016/0022-5193(82)90225-9)

ParkerGA 1984 Sperm competition and the evolution of animal mating systems. In Sperm Competition and the Evolution of Animal Mating Systems pp 160. Ed SmithRL. San Diego: Academic Press.

ParkerGA 1993 Sperm competition games: sperm size and sperm number under adult control. Proceedings of the Royal Society B 253 245254. (https://doi.org/10.1098/rspb.1993.0110)

ParkerGA 2006 Sexual conflict over mating and fertilization: an overview. Philosophical Transactions of the Royal Society of London B 361 235259. (https://doi.org/10.1098/rstb.2005.1785)

ParkerGA 2014 The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. Cold Spring Harbor Perspectives in Biology 6 a017509. (https://doi.org/10.1101/cshperspect.a017509)

ParkerGAPizzariT 2010 Sperm competition and ejaculate economics. Biological Reviews 85 897934. (https://doi.org/10.1111/j.1469-185X.2010.00140.x)

ParkerGABakerRRSmithVG 1972 The origin and evolution of gamete dimorphism and the male-female phenomenon. Journal of Theoretical Biology 36 529553. (https://doi.org/10.1016/0022-5193(72)90007-0)

ParkerGAImmlerSPitnickSBirkheadTR 2010 Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. Journal of Theoretical Biology 264 10031023. (https://doi.org/10.1016/j.jtbi.2010.03.003)

PartridgeLHoffmannAJonesJS 1987 Male size and mating success in Drosophila melanogaster and D. pseudoobscura under field conditions. Animal Behaviour 35 468476. (https://doi.org/10.1016/S0003-3472(87)80272-5)

PattariniJMStarmerWTBjorkAPitnickS 2006 Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60 20642080. (https://doi.org/10.1111/j.0014-3820.2006.tb01844.x)

PerettiAVEberhardWG 2010 Cryptic female choice via sperm dumping favours male copulatory courtship in a spider. Journal of Evolutionary Biology 23 2712781. (https://doi.org/10.1111/j.1420-9101.2009.01900.x)

PerryJCRoweL 2010 Condition-dependent ejaculate size and composition in a ladybird beetle. Proceedings of the Royal Society B 277 36393647. (https://doi.org/10.1098/rspb.2010.0810)

PhillipsDM 1966 Fine structure of Sciara coprophila sperm. Journal of Cell Biology 30 499517. (https://doi.org/10.1083/jcb.30.3.499)

PitnickS 1996 Investment in testes and the cost of making long sperm in Drosophila. American Naturalist 148 5780. (https://doi.org/10.1086/285911)

PitnickSBrownWD 2000 Criteria for demonstrating female sperm choice. Evolution 54 10521056. (https://doi.org/10.1111/j.0014-3820.2000.tb00107.x)

PitnickSSpicerGSMarkowTA 1995 How long is a giant sperm? Nature 375 109. (https://doi.org/10.1038/375109a0)

PitnickSSMarkowTASpicerGS 1999 Evolution of multiple kinds of female sperm-storage organs in Drosophila. Evolution 53 18041822. (https://doi.org/10.1111/j.1558-5646.1999.tb04564.x)

PitnickSHoskenDJBirkheadTR 2009a Sperm morphological diversity. In Sperm Biology: An Evolutionary Perspective pp 69149. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

PitnickSWolfnerMFSuarezSS 2009b Ejaculate-female and sperm-female interactions. In Sperm Biology: An Evolutionary Perspective pp 247304. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

PizzariTBirkheadTR 2000 Female feral fowl eject sperm of subdominant males. Nature 405 787789. (https://doi.org/10.1038/35015558)

PizzariTParkerGA 2009 Sperm competition and sperm phenotype. In Sperm Biology: An Evolutionary Perspective pp 207245. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

PoianiA 2006 Complexity of seminal fluid: a review. Behavioral Ecology and Sociobiology 60 289310. (https://doi.org/10.1007/s00265-006-0178-0)

PresgravesDCBakerRHWilkinsonGS 1999 Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proceedings of the Royal Society B 266 10411047. (https://doi.org/10.1098/rspb.1999.0741)

PuniamoorthyNKotrbaMMeierR 2010 Unlocking the ‘Black box’: internal female genitalia in Sepsidae (Diptera) evolve fast and are species-specific. BMC Evolutionary Biology 10 275. (https://doi.org/10.1186/1471-2148-10-275)

RahmanMMKelleyJLEvansJP 2013 Condition-dependent expression of pre- and postcopulatory sexual traits in guppies. Ecology and Evolution 3 21972213. (https://doi.org/10.1002/ece3.632)

Ravi RamKWolfnerMF 2007 Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integrative and Comparative Biology 47 427445. (https://doi.org/10.1093/icb/icm046)

ReinhardtKDoblerRAbbottJ 2015 An ecology of sperm: sperm diversification by natural selection. Annual Review of Ecology Evolution and Systematics 46 435459. (https://doi.org/10.1146/annurev-ecolsys-120213-091611)

RosengravePGemmellNJMetcalfVMcBrideKMontgomerieR 2008 A mechanism for cryptic female choice in chinook salmon. Behavioral Ecology 19 11791185. (https://doi.org/10.1093/beheco/arn089)

RoweLHouleD 1996 The lek paradox and the capture of genetic variance by condition dependent traits. Proceedings of the Royal Society B 263 14151421. (https://doi.org/10.1098/rspb.1996.0207)

Rugman-JonesPFEadyPE 2008 Co-evolution of male and female reproductive traits across the Bruchidae (Coleoptera). Functional Ecology 22 880886. (https://doi.org/10.1111/j.1365-2435.2008.01446.x)

RyanMJ 1990 Sexual selection, sensory systems and sensory exploitation. Oxford Surveys in Evolutionary Biology 7 157195.

SasanamiTMatsuzakiMMizushimaSHiyamaG 2013 Sperm storage in the female reproductive tract in birds. Journal of Reproduction and Development 59 334338. (https://doi.org/10.1262/jrd.2013-038)

SchärerLJossGSandnerP 2004 Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Marine Biology 145 373380. (https://doi.org/10.1007/s00227-004-1314-x)

SchärerLLittlewoodDTJWaeschenbachAYoshidaWVizosoDB 2011 Mating behavior and the evolution of sperm design. PNAS 108 14901495. (https://doi.org/10.1073/pnas.1013892108)

SchnakenbergSLSiegalMLBloch QaziMC 2012 Oh, the places they’ll go: female sperm storage and sperm precedence in Drosophila melanogaster. Spermatogenesis 2 224235. (https://doi.org/10.4161/spmg.21655)

SheldonBC 1994 Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proceedings of the Royal Society B 257 2530. (https://doi.org/10.1098/rspb.1994.0089)

SimmonsLWFitzpatrickJL 2012 Sperm wars and the evolution of male fertility. Reproduction 144 519534. (https://doi.org/10.1530/REP-12-0285)

SimmonsLWMooreAJ 2009 Evolutionary quantitative genetics of sperm. In Sperm Biology: An Evolutionary Perspective pp 405434. Eds BirkheadTRHoskenDJ & PitnickS. San Diego: Academic Press.

SimmonsLWSiva-JothyMT 1998 Sperm competition in insects: mechanisms and the potential for selection. In Sperm Competition and Sexual Selection pp 341434. Eds BirkheadTR & MøllerAP. London: Academic Press.

SimmonsLWRobertsJDDziminskiMA 2009 Egg jelly influences sperm motility in the externally fertilizing frog, Crinia georgiana. Journal of Evolutionary Biology 22 225229. (https://doi.org/10.1111/j.1420-9101.2008.01628.x)

SimpsonJLHumphriesSEvansJPSimmonsLWFitzpatrickJL 2014 Relationships between sperm length and speed differ among three internally and three externally fertilizing species. Evolution 68 92104. (https://doi.org/10.1111/evo.12199)

SivinskiJ 1984 Sperm in competition. In Sperm Competition and the Evolution of Animal Mating Systems pp 85115. Ed SmithRL. New York: Academic Press.

SmithRJMatzke-KaraszRKamiyaTDe DeckkerP 2016 Sperm lengths of non-marine cypridoidean ostracods (Crustacea). Acta Zoologica 97 117. (https://doi.org/10.1111/azo.12099)

SnookRR 2005 Sperm in competition: not playing by the numbers. Trends in Ecology and Evolution 20 4653. (https://doi.org/10.1016/j.tree.2004.10.011)

SnookRRHoskenDJ 2004 Sperm death and dumping in Drosophila. Nature 428 939941. (https://doi.org/10.1038/nature02455)

StivalCPuga MolinaLCPaudelBBuffoneMGViscontiPEKrapfD 2016 Sperm capacitation and acrosome reaction in mammalian sperm. Advances in Anatomy Embryology and Cell Biology 220 93106. (https://doi.org/10.1007/978-3-319-30567-7_5)

StockleyPGageMJGParkerGAMøllerAP 1996 Female reproductive biology and the coevolution of ejaculate characteristics in fish. Proceedings of the Royal Society of London B 263 451458. (https://doi.org/10.1098/rspb.1996.0068)

StockleyPGageMJGParkerGAMøllerAP 1997 Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. American Naturalist 149 933954. (https://doi.org/10.1086/286031)

SuarezSSHoHC 2003 Hyperactivation of mammalian sperm. Cellular and Molecular Biology 49 351356.

SuarezSSPaceyAA 2006 Sperm transport in the female reproductive tract. Human Reproduction Update 12 2337. (https://doi.org/10.1093/humupd/dmbib47)

TemkinMHBortolamiSB 2004 Waveform dynamics of spermatozeugmata during the transfer from paternal to maternal individuals of Membranipora membranacea. Biological Bulletin 206 3545. (https://doi.org/10.2307/1543196)

ThomsenRSoltisJMatsubaraMMatsubayashiKOnumaMTakenakaO 2006 How costly are ejaculates for Japanese macaques? Primates 47 272274. (https://doi.org/10.1007/s10329-005-0171-7)

ThornhillR 1983 Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. American Naturalist 122 765788. (https://doi.org/10.1086/284170)

TingJJWoodruffGCLeungGShinN-RCutterADHaagES 2014 Intense sperm-mediated sexual conflict promotes reproductive isolation in Caenorhabditis nematodes. PLoS Biology 12 e1001915. (https://doi.org/10.1371/journal.pbio.1001915)

TobiasJAMontgomerieRLyonBE 2012 The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philosophical Transactions of the Royal Society of London B 367 22742293. (https://doi.org/10.1098/rstb.2011.0280)

TomkinsJLRadwanJKotiahoJSTregenzaT 2004 Genic capture and resolving the lek paradox. Trends in Ecology and Evolution 19 323328. (https://doi.org/10.1016/j.tree.2004.03.029)

TourmenteMGomendioMRoldanERS 2011 Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals. PLoS ONE 6 e21244. (https://doi.org/10.1371/journal.pone.0021244)

TriversRL 1972 Parental investment and sexual selection. In Sexual Selection and the Descent of Man 1871–1971 pp 136179. Ed CampbellB. Chicago, IL: Aldine-Atherton.

TurnerEMontgomerieR 2002 Ovarian fluid enhances sperm movement in Arctic charr. Journal of Fish Biology 60 15701579. (https://doi.org/10.1111/j.1095-8649.2002.tb02449.x)

Veiga-MenoncelloACAguiarOJrLimaAPRecco-PimentelSM 2007 The biflagellate spermatozoa of Colostethus marchesianus (Melin 1941) (Anura Dendrobatidae) from the type locality and Colostethus sp (aff marchesianus) from a different locality: A scanning and transmission electron microscopy analysis. Zoolischer Anzeiger 246 4959. (https://doi.org/10.1016/j.jcz.2006.12.001)

WaageJK 1979 Dual function of the damselfly penis: sperm removal and transfer. Science 203 916918. (https://doi.org/10.1126/science.203.4383.916)

WadeMJArnoldSJ 1980 The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Animal Behaviour 28 446461. (https://doi.org/10.1016/S0003-3472(80)80052-2)

WagnerRHHelfensteinFDanchinE 2004 Female choice of young sperm in a genetically monogamous bird. Proceedings of the Royal Society B 271 S134S137. (https://doi.org/10.1098/rsbl.2003.0142)

WileyRHPostonJ 1996 Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50 13711381. (https://doi.org/10.1111/j.1558-5646.1996.tb03911.x)

WilsonNTubmanSCEadyPERobertsonGW 1997 Female genotype affects male success in sperm competition. Proceedings of the Royal Society B 264 14911495. (https://doi.org/10.1098/rspb.1997.0206)

WingstrandKG 1988 Comparative spermatology of the CrustaceaEntomostraca. 2 Subclass Ostracoda. Biologiske Skrifter 32 1149.

WolfnerMF 2011 Precious essences: female secretions promote sperm storage in Drosophila. PLoS Biology 9 e1001191. (https://doi.org/10.1371/journal.pbio.1001191)

WoolleyDM 2003 Motility of spermatozoa at surfaces. Reproduction 126 259270. (https://doi.org/10.1530/rep.0.1260259)

YasuiY 1997 A ‘good-sperm’ model can explain the evolution of multiple mating by females. American Naturalist 149 573584. (https://doi.org/10.1086/286006)

YeatesSEDiamondSEEinumSEmersonBCHoltWVGageMJG 2013 Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior. Evolution 67 35233536. (https://doi.org/10.1111/evo.12208)

YoshidaMKawanoNYoshidaK 2008 Control of sperm motility and fertility: diverse factors and common mechanisms. Cellular and Molecular Life Sciences 65 34463457. (https://doi.org/10.1007/s00018-008-8230-z)

YoshidaMHiradateYSensuiNCossonJMorisawaM 2013 Species-specificity of sperm motility activation and chemotaxis: a study on ascidian species. Biological Bulletin 224 156165. (https://doi.org/10.1086/BBLv224n3p156)

ZhangYZZhangSCLiuXZXuYYWangCLSawantMSLiJChenSL2003 Cryopreservation of flounder (Paralichthys olivaceus) sperm with a practical methodology. Theriogenology 60 989996. (https://doi.org/10.1038/srep16096)

ZhangLYangPBianXZhangQUllahSWaqasYChenXLiuYChenWLeY 2015 Modification of sperm morphology during long-term sperm storage in the reproductive tract of the Chinese soft-shelled turtle, Pelodiscus sinensis. Scientific Reports 5 16096. (https://doi.org/10.1038/srep16096)

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