Skip to main content
Log in

Strategic adjustment of ejaculate quality in response to variation of the socio-sexual environment

  • Review
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Strategic ejaculate adjustments occur when males modify their investment in sperm and nonsperm components of the ejaculate according to the context. This strategy is expected to evolve when ejaculate production is costly, the returns of the investment in the ejaculate depend on the environment and environmental conditions are variable. While adjustments of sperm numbers have been widely documented, only recently we have begun to investigate how males modify ejaculate quality, despite the recognized importance of this factor for sperm competition. Here I discuss and synthetize existing literature on strategic adjustments of ejaculate quality. I describe which ejaculate quality traits are most typically plastic and which environmental factors elicit such responses, focusing especially on the socio-sexual environment. I summarize information on the timeframe within which adjustments can occur and on the proximate mechanisms responsible for plasticity. I show that this phenomenon is widespread across taxa; it involves responses to several environmental factors and modifications of many ejaculate traits, with seminal fluid composition playing a central role, as a trait per se and as proximate mechanism for sperm performance adjustments. I point out the circumstances favoring the evolution of ejaculate quality plasticity, and evaluate the fitness consequences of these responses, highlighting the complexity of patterns of covariation with other traits. Finally, I consider implications for male and female behavior. I highlight two areas of research on ejaculate plasticity that may be particularly worth exploring further: 1) the proximate mechanisms responsible for plasticity; 2) the adaptive value of strategic ejaculate adjustments.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abe J, Kamimura Y (2015) Sperm economy between female mating frequency and male ejaculate allocation. Am Nat 185:406–416

    PubMed  Google Scholar 

  • Adler MI, Bonduriansky R (2013) Paternal effects on offspring fitness reflect father’s social environment. Evol Biol 40:288–292

    Google Scholar 

  • Alonzo SH, Pizzari T (2010) Male fecundity stimulation: conflict and cooperation within and between the sexes: model analyses and coevolutionary dynamics. Am Nat 175:174–185

    PubMed  Google Scholar 

  • Alonzo SH, Stiver KA, Marsh-Rollo SE (2016) Ovarian fluid allows directional cryptic female choice despite external fertilization. Nat Commun 7:12452

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alvarez-Fernandez A, Borziak K, McDonald GC, Dorus S, Pizzari T (2019) Female novelty and male status dynamically modulate ejaculate expenditure and seminal fluid proteome over successive matings in red junglefowl. Sci Rep 9:5852. https://doi.org/10.1038/s41598-019-41336-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apostólico LH, Marian JEAR (2017) Dimorphic ejaculates and sperm release strategies associated with alternative mating behaviors in the squid. J Morphol 278:1490–1505

    PubMed  Google Scholar 

  • Apostólico LH, Marian JEAR (2018) Dimorphic male squid show differential gonadal and ejaculate expenditure. Hydrobiologia 808:5–22

    Google Scholar 

  • Arundell KL, Wedell N, Dunn AM (2014) Perceived risk of sperm competition affects sperm investment in a mate-guarding amphipod. Anim Behav 87:231–238

    Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc Lond B 277:503–511. https://doi.org/10.1098/rspb.2009.1355

    Article  Google Scholar 

  • Barbosa F (2012) Males responding to sperm competition cues have higher fertilization success in a soldier fly. Behav Ecol 23:815–819. https://doi.org/10.1093/beheco/ars035

    Article  Google Scholar 

  • Bartlett MJ, Steeves TE, Gemmell NJ, Rosengrave PC (2017) Sperm competition risk drives rapid ejaculate adjustments mediated by seminal fluid. Elife 6:e28811

    PubMed  PubMed Central  Google Scholar 

  • Bateson P, Barker D, Clutton-Brock T et al (2004) Developmental plasticity and human health. Nature 430:419–421

    CAS  PubMed  Google Scholar 

  • Bayram HL, Franco C, Brownridge P, Claydon AJ, Koch N, Hurst JL, Beynon RJ, Stockley P (2020) Social status and ejaculate composition in the house mouse. Philos Trans R Soc B 375:20200083 https://doi.org/10.1098/rstb.2020.0083

    CAS  Google Scholar 

  • Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, London

    Google Scholar 

  • Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764

    CAS  Google Scholar 

  • Bjork A, Dallai R, Pitnick S (2007) Adaptive modulation of sperm production rate in Drosophila bifurca, a species with giant sperm. Biol Lett 3:517–519

    PubMed  PubMed Central  Google Scholar 

  • Bonilla MM, Zeh DW, White AM, Zeh JA (2011) Discriminating males and unpredictable females: males bias sperm allocation in favor of virgin females. Ethology 117:740–748

    Google Scholar 

  • Boschetto C, Gasparini C, Pilastro A (2011) Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 65:813–821. https://doi.org/10.1007/s00265-010-1085-y

    Article  Google Scholar 

  • Bozynski CC, Liley NR (2003) The effect of female presence on spermiation, and of male sexual activity on ‘ready’ sperm in the male guppy. Anim Behav 65:53–58. https://doi.org/10.1006/anbe.2002.2024

    Article  Google Scholar 

  • Bretman A, Newcombe D, Tregenza T (2009) Promiscuous females avoid inbreeding by controlling sperm storage. Mol Ecol 18:3340–3345. https://doi.org/10.1111/j.1365-294X.2009.04301.x

    Article  PubMed  Google Scholar 

  • Bretman A, Westmancoat JD, Gage MJ, Chapman T (2011) Males use multiple, redundant cues to detect mating rivals. Curr Biol 21:617–622

    CAS  PubMed  Google Scholar 

  • Bretman A, Westmancoat JD, Gage MJG, Chapman T (2013) Costs and benefits of lifetime exposure to mating rivals in male Drosophila melanogaster. Evolution 67:2413–2422

    PubMed  Google Scholar 

  • Bretman A, Fricke C, Westmancoat JD, Chapman T (2016) Effect of competitive cues on reproductive morphology and behavioral plasticity in male fruitflies. Behav Ecol 27:452–461

    PubMed  Google Scholar 

  • Burger D, Dolivo G, Marti E, Sieme H, Wedekind C (2015a) Female major histocompatibility complex type affects male testosterone levels and sperm number in the horse (Equus caballus). Proc R Soc B 282:20150407

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burger D, Dolivo G, Wedekind C (2015b) Ejaculate characteristics depend on social environment in the horse (Equus caballus). PLoS ONE 10:e0143185

    PubMed  PubMed Central  Google Scholar 

  • Burness G, Casselman SJ, Schulte-Hostedde AI, Cd M, Montgomery R (2004) Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav Ecol Sociobiol 56:65–70. https://doi.org/10.1007/s00265-003-0752-7

    Article  Google Scholar 

  • Cameron E, Day T, Rowe L (2007) Sperm competition and the evolution of ejaculate composition. Am Nat 169:E158–E172. https://doi.org/10.1086/516718

    Article  PubMed  Google Scholar 

  • Cardozo G, Devigili A, Antonelli P, Pilastro A (2020) Female sperm storage mediates costs and benefits of ejaculate anticipatory plasticity in the guppy. J Evol Biol 33:1294–1305

    PubMed  Google Scholar 

  • Cattelan S, Evans JP, Pilastro A, Gasparini C (2016) The effect of sperm production and mate availability on patterns of alternative mating tactics in the guppy. Anim Behav 112:105–110

    Google Scholar 

  • Claydon AJ, Ramm SA, Pennington A, Hurst JL, Stockley P, Beynon R (2012) Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labeling. Mol Cell Proteomics 11:M111. 014993

    PubMed  PubMed Central  Google Scholar 

  • Cook PA, Gage MJG (1995) Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae). Behav Ecol Sociobiol 36:261–268

    Google Scholar 

  • Cook PA, Wedell N (1996) Ejaculate dynamics in butterflies: a strategy for maximizing fertilization success? Proc R Soc Lond B 263:1047–1051

    Google Scholar 

  • Cook PA, Wedell N (1999) Non-fertile sperm delay female remating. Nature 397:486. https://doi.org/10.1038/17257

    Article  CAS  Google Scholar 

  • Cornwallis CK, Birkhead TR (2007) Changes in sperm quality and numbers in response to experimental manipulation of male social status and female attractiveness. Am Nat 170:758–770. https://doi.org/10.1086/521955

    Article  PubMed  Google Scholar 

  • Cornwallis CK, Birkhead TR (2008) Plasticity in reproductive phenotypes reveals status-specific correlations between behavioral, morphological, and physiological sexual traits. Evolution 62:1149–1161

    PubMed  Google Scholar 

  • Cornwallis CK, O’Connor EA (2009) Sperm: seminal fluid interactions and the adjustment of sperm quality in relation to female attractiveness. Proc R Soc Lond B 276:3467–3475. https://doi.org/10.1098/rspb.2009.0807

    Article  Google Scholar 

  • Crean AJ, Marshall DJ (2008) Gamete plasticity in a broadcast spawning marine invertebrate. P Natl Acad Sci USA 105:13508–13513. https://doi.org/10.1073/pnas.0806590105

    Article  Google Scholar 

  • Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology 94:2575–2582

    PubMed  Google Scholar 

  • Crean AJ, Kopps AM, Bonduriansky R (2014) Revisiting telegony: offspring inherit an acquired characteristic of their mother’s previous mate. Ecol Lett 17:1545–1552

    PubMed  PubMed Central  Google Scholar 

  • Crean AJ, Adler MI, Bonduriansky R (2016) Seminal fluid and mate choice: new predictions. Trends Ecol Evol 31:253–255

    PubMed  Google Scholar 

  • Dasgupta P, Halder S, Nandy B (2016) Paternal social experience affects male reproductive behaviour in Drosophila melanogaster. J Genet 95:725–727

    CAS  PubMed  Google Scholar 

  • Daye PG, Glebe BD (1984) Fertilization success and sperm motility of Atlantic salmon (Salmo salar L.) in acidified water. Aquaculture 43:307–312

    Google Scholar 

  • delBarco-Trillo J (2011) Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J Evol Biol 24:1706–1714

    CAS  PubMed  Google Scholar 

  • delBarco-Trillo J, Garcia-Alvarez O, Soler AJ, Tourmente M, Garde JJ, Roldan ER (2016) A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation. Proc R Soc B 283:20152708

    PubMed  PubMed Central  Google Scholar 

  • den Boer SPA, Baer B, Boomsma JJ (2010) Seminal fluid mediates ejaculate competition in social insects. Science 327:1506–1509

    Google Scholar 

  • Denk AG, Holzmann A, Peters A, Vermeirssen EL, Kempenaers B (2005) Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16:825–833

    Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    CAS  PubMed  Google Scholar 

  • Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610

    Google Scholar 

  • Dowling DK, Simmons LW (2012) Ejaculate economics: testing the effects of male sexual history on the trade-off between sperm and immune function in Australian crickets. PLoS ONE 7:e30172

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dresdner RD, Katz DF (1981) Relationships of mammalian sperm motility and morphology to hydrodynamic aspects of cell function. Biol Reprod 25:920–930

    CAS  PubMed  Google Scholar 

  • Dziuk PJ (1996) Factors that influence the proportion of offspring sired by a male following heterospermic insemination. Anim Reprod Sci 43:65–88

    Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Egeland TB, Rudolfsen G, Nordeide JT, Folstad I (2015) On the relative effect of spawning asynchrony, sperm quantity, and sperm quality on paternity under sperm competition in an external fertilizer. Front Ecol Evol 3:77. https://doi.org/10.3389/fevo.2015.00077

    Article  Google Scholar 

  • Egeland TB, Rudolfsen G, Nordeide JT, Folstad I (2016) Status specific tailoring of sperm behavior in an external fertilizer. Front Ecol Evol 4:135

    Google Scholar 

  • Eisenberg DTA (2011) An evolutionary review of human telomere biology: the thrifty telomere hypothesis and notes on potential adaptive paternal effects. Am J Hum Biol 23:149–167

    PubMed  Google Scholar 

  • Engqvist L, Reinhold K (2005) Pitfalls in experiments testing predictions from sperm competition theory. J Evol Biol 18:116–123. https://doi.org/10.1111/j.1420-9101.2004.00792.x

    Article  CAS  PubMed  Google Scholar 

  • Engqvist L, Reinhold K (2006) Theoretical influence of female mating status and remating propensity on male sperm allocation patterns. J Evol Biol 19:1448–1458

    CAS  PubMed  Google Scholar 

  • Evans JP (2009) No evidence for sperm priming responses under varying sperm competition risk or intensity in guppies. Naturwissenschaften 96:771–779. https://doi.org/10.1007/s00114-009-0529-6

    Article  CAS  PubMed  Google Scholar 

  • Evans JP, Garcia-Gonzalez F (2016) The total opportunity for sexual selection and the integration of pre-and post-mating episodes of sexual selection in a complex world. J Evol Biol 29:2338–2361

    CAS  PubMed  Google Scholar 

  • Fasel NJ, Wesseling C, Fernandez AA, Vallat A, Glauser G, Helfenstein F, Richner H (2017) Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat). Behav Ecol Sociobiol 71:11. https://doi.org/10.1007/s00265-016-2251-7

    Article  Google Scholar 

  • Fedorka KM, Winterhalter WE, Ware B (2011) Perceived sperm competition intensity influences seminal fluid protein production prior to courtship and mating. Evolution 65:584–590. https://doi.org/10.1111/j.1558-5646.2010.01141.x

    Article  PubMed  Google Scholar 

  • Filice DCS, Dukas R (2019) Winners have higher pre-copulatory mating success but losers have better post-copulatory outcomes. Proc R Soc B 286:20182838

    CAS  PubMed  PubMed Central  Google Scholar 

  • Filice DCS, Bhargava R, Dukas R (2020) Plasticity in male mating behavior modulates female life history in fruit flies. Evolution 74:365–376. https://doi.org/10.1111/evo.13926

    Article  PubMed  Google Scholar 

  • Firman RC, Garcia-Gonzalez F, Simmons LW, André GI (2018) A competitive environment influences sperm production, but not testes tissue composition, in house mice. J Evol Biol 31:1647–1654

    PubMed  Google Scholar 

  • Firman RC, Tedeschi JN, Garcia-Gonzalez F (2020) Sperm sex ratio adjustment in a mammal: perceived male competition leads to elevated proportions of female-producing sperm. Biol Lett 16:20190929

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fitzpatrick JL, Lüpold S (2014) Sexual selection and the evolution of sperm quality. Mol Hum Reprod 20:1180–1189. https://doi.org/10.1093/molehr/gau067

    Article  PubMed  Google Scholar 

  • Fitzpatrick JL, Desjardins JK, Milligan N, Montgomery R, Balshine S (2007) Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol Reprod 77:280–284. https://doi.org/10.1095/biolreprod.106.059550

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick LJ, Gasparini C, Fitzpatrick JL, Evans JP (2014) Male–female relatedness and patterns of male reproductive investment in guppies. Biol Lett 10:20140166

    PubMed  PubMed Central  Google Scholar 

  • Fitzpatrick JL, Earn DJD, Bucking C, Craig PM, Nadella S, Wood CM, Balshine S (2016) Postcopulatory consequences of female mate choice in a fish with alternative reproductive tactics. Behav Ecol 27:312–320. https://doi.org/10.1093/beheco/arv159

    Article  Google Scholar 

  • Flannery EW, Butts IAE, Słowińska M, Ciereszko A, Pitcher TE (2013) Reproductive investment patterns, sperm characteristics, and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tshawytscha). Biol J Linn Soc 108:99–108

    Google Scholar 

  • Franz Schrader, (1960) EVOLUTIONARY ASPECTS OF ABERRANT MEIOSIS IN SOME PENTATOMINAE (HETEROPTERA). Evolution 14 (4):498-508

  • Friedländer M (1997) Control of the eupyrene–apyrene sperm dimorphism in lepidoptera. J Insect Physiol 43:1085–1092

    PubMed  Google Scholar 

  • Friedländer M, Hauschteck-Jungen E (1982) Differential basic nucleoprotein kinetics in the two kinds of Lepidoptera spermatids: nucleate (eupyrene) and anucleate (apyrene). Chromosoma 85:387–398

    PubMed  Google Scholar 

  • Friesen CR, Powers DR, Copenhaver PE, Mason RT (2015) Size dependence in non-sperm ejaculate production is reflected in daily energy expenditure and resting metabolic rate. J Exp Biol 218:1410–1418

    PubMed  Google Scholar 

  • Fusco G, Minelli A (2010) Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc B 365:547–556

    Google Scholar 

  • Gage MJG (1995) Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc R Soc Lond B 261:25–30

    Google Scholar 

  • Gage MJG, Stockley P, Parker GA (1995) Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations. Philos Trans R Soc Lond B 350:391–399. https://doi.org/10.1098/rstb.1995.0173

    Article  Google Scholar 

  • Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136

    CAS  PubMed  Google Scholar 

  • Garcia-Gonzalez F, Dowling DK (2015) Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation. Biol Lett 11:20150067

    PubMed  PubMed Central  Google Scholar 

  • García-González F, Simmons LW (2005) Sperm viability matters in insect sperm competition. Curr Biol 15:271–275. https://doi.org/10.1016/j.cub.2005.01.032

    Article  CAS  PubMed  Google Scholar 

  • Gasparini C, Peretti AV, Pilastro A (2009) Female presence influences sperm velocity in the guppy. Biol Lett 5:792–794. https://doi.org/10.1098/rsbl.2009.0413

    Article  PubMed  PubMed Central  Google Scholar 

  • Gasparini C, Devigili A, Dosselli R, Pilastro A (2013) Pattern of inbreeding depression, condition dependence, and additive genetic variance in Trinidadian guppy ejaculate traits. Ecol Evol 3:4940–4953. https://doi.org/10.1002/ece3.870

    Article  PubMed  PubMed Central  Google Scholar 

  • Gasparini C, Dosselli R, Evans JP (2017) Sperm storage by males causes changes in sperm phenotype and influences the reproductive fitness of males and their sons. Evol Lett 1:16–25

    PubMed  PubMed Central  Google Scholar 

  • Gasparini C, Pilastro A, Evans JP (2020) The role of female reproductive fluid in sperm competition. Philos Trans R Soc B 375:20200077. https://doi.org/10.1098/rstb.2020.0077

    Article  CAS  Google Scholar 

  • Giannakara A, Scharer L, Ramm SA (2016) Sperm competition-induced plasticity in the speed of spermatogenesis. BMC Evol Biol 16:60. https://doi.org/10.1186/s12862-016-0629-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gombar R, Pitcher TE, Lewis JA, Auld J, Vacratsis PO (2017) Proteomic characterization of seminal plasma from alternative reproductive tactics of Chinook salmon (Oncorhynchus tswatchysha). J Proteome 157:1–9

    CAS  Google Scholar 

  • Gowaty PA (2003) Power asymmetries between the sexes, mate preferences, and components of fitness. In: Travis CB (ed) Evolution, gender, and rape. MIT Press, Cambridge, pp 61–86

    Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    CAS  PubMed  Google Scholar 

  • Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101

    CAS  PubMed  Google Scholar 

  • Hadlow JH, Evans JP, Lymbery RA (2020) Egg-induced changes to sperm phenotypes shape patterns of multivariate selection on ejaculates. J Evol Biol (published online. https://doi.org/10.1111/jeb.13611)

  • Harris WE, Moore PJ (2005) Sperm competition and male ejaculate investment in Nauphoeta cinerea: effects of social environment during development. J Evol Biol 18:474–480. https://doi.org/10.1111/j.1420-9101.2004.00816.x

    Article  CAS  PubMed  Google Scholar 

  • Haugland T, Rudolfsen G, Figenschou L, Folstad I (2009) Sperm velocity and its relation to social status in Arctic charr (Salvelinus alpinus). Anim Reprod Sci 115:231–237

    PubMed  Google Scholar 

  • Hayakawa Y (2007) Parasperm: morphological and functional studies on nonfertile sperm. Ichthyol Res 54:111–130

    Google Scholar 

  • He Y, Miyata T (1997) Variations in sperm number in relation to larval crowding and spermatophore size in the armyworm, Pseudaletia separata. Ecol Entomol 22:41–46. https://doi.org/10.1046/j.1365-2311.1997.00030.x

    Article  Google Scholar 

  • Herberstein ME, Schneider JM, Harmer AMT et al (2011) Sperm storage and copulation duration in a sexually cannibalistic spider. J Ethol 29:9–15. https://doi.org/10.1007/s10164-010-0213-5

    Article  Google Scholar 

  • Hirohashi N, Iwata Y (2013) The different types of sperm morphology and behavior within a single species: Why do sperm of squid sneaker males form a cluster? Commun Integr Biol 6:e26729

    PubMed  PubMed Central  Google Scholar 

  • Hirohashi N, Alvarez L, Shiba K et al (2013) Sperm from sneaker male squids exhibit chemotactic swarming to CO2. Curr Biol 23:775–781

    CAS  PubMed  Google Scholar 

  • Hirohashi N, Tamura-Nakano M, Nakaya F, Iida T, Iwata Y (2016) Sneaker male squid produce long-lived spermatozoa by modulating their energy metabolism. J Biol Chem 291:19324–19334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hodgson DJ, Hosken DJ (2006) Sperm competition promotes the exploitation of rival ejaculates. J Theor Biol 243:230–234. https://doi.org/10.1016/j.jtbi.2006.06.024

    Article  CAS  PubMed  Google Scholar 

  • Holman L, Snook RR (2008) A sterile sperm caste protects brother fertile sperm from female-mediated death in Drosophila pseudoobscura. Curr Biol 18:292–296. https://doi.org/10.1016/j.cub.2008.01.048

    Article  CAS  PubMed  Google Scholar 

  • Hopkins BR, Sepil I, Thézénas M-L et al (2019) Divergent allocation of sperm and the seminal proteome along a competition gradient in Drosophila melanogaster. P Natl Acad Sci USA 116:17925–17933

    CAS  Google Scholar 

  • Hoysak DJ, Liley NR (2001) Fertilization dynamics in sockeye salmon and a comparison of sperm from alternative male phenotypes. J Fish Biol 58:1286–1300

    Google Scholar 

  • Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319. https://doi.org/10.1186/1471-2148-8-319

    Article  PubMed  PubMed Central  Google Scholar 

  • Hunt J, Breuker CJ, Sadowski JA, Moore AJ (2009) Male–male competition, female mate choice and their interaction: determining total sexual selection. J Evol Biol 22:13–26

    PubMed  Google Scholar 

  • Hunter FM, Birkhead TR (2002) Sperm viability and sperm competition in insects. Curr Biol 12:121–123

    CAS  PubMed  Google Scholar 

  • Immler S (2018) The sperm factor: paternal impact beyond genes. Heredity 121:239–247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643. https://doi.org/10.1111/j.1558-5646.2009.00924.x

    Article  PubMed  Google Scholar 

  • Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. P Natl Acad Sci USA 108:5325–5330

    CAS  Google Scholar 

  • Iwata Y, Shaw P, Fujiwara E, Shiba K, Kakiuchi Y, Hirohashi N (2011) Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours. BMC Evol Biol 11:236

    PubMed  PubMed Central  Google Scholar 

  • Janicke T, Schärer L (2010) Sperm competition affects sex allocation but not sperm morphology in a flatworm. Behav Ecol Sociobiol 64:1367–1375

    Google Scholar 

  • Janicke T, Sandner P, Ramm SA, Vizoso DB, Schärer L (2016) Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm. J Evol Biol 29:1713–1727

    CAS  PubMed  Google Scholar 

  • Jeannerat E, Janett F, Sieme H, Wedekind C, Burger D (2017) Quality of seminal fluids varies with type of stimulus at ejaculation. Sci Rep 7:44339

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeannerat E, Marti E, Berney C, Janett F, Bollwein H, Sieme H, Burger D, Wedekind C (2018) Stallion semen quality depends on MHC matching to teaser mare. Mol Ecol 27:1025–1035

    CAS  PubMed  Google Scholar 

  • Jewgenow K, Neubauer K, Blottner S, Schön J, Wildt DE, Pukazhenthi BS (2009) Reduced germ cell apoptosis during spermatogenesis in the teratospermic domestic cat. J Androl 30:460–468

    CAS  PubMed  Google Scholar 

  • Joseph PN, Sharma RK, Agarwal A, Sirot LK (2015) Men ejaculate larger volumes of semen, more motile sperm, and more quickly when exposed to images of novel women. Evol Psychol Sci 1:195–200. https://doi.org/10.1007/s40806-015-0022-8

    Article  Google Scholar 

  • Kasumovic MM (2013) The multidimensional consequences of the juvenile environment: towards an integrative view of the adult phenotype. Anim Behav 85:1049–1059. https://doi.org/10.1016/j.anbehav.2013.02.009

    Article  Google Scholar 

  • Kasumovic MM, Brooks RC (2011) It’s all who you know: the evolution of socially cued anticipatory plasticity as a mating strategy. Q Rev Biol 86:181–197

    PubMed  Google Scholar 

  • Kelly CD, Jennions MD (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol Rev 86:863–884. https://doi.org/10.1111/j.1469-185X.2011.00175.x

    Article  PubMed  Google Scholar 

  • Kerwin P, von Philipsborn AC (2020) Copulation song in Drosophila: do females sing to change male ejaculate allocation and incite postcopulatory mate choice? BioEssays 42:2000109

    Google Scholar 

  • Kilgallon SJ, Simmons LW (2005) Image content influences men’s semen quality. Biol Lett 1:253–255. https://doi.org/10.1098/rsbl.2005.0324

    Article  PubMed  PubMed Central  Google Scholar 

  • Koyama S, Kamimura S (2000) Influence of social dominance and female odor on the sperm activity of male mice. Physiol Behav 71:415–422

    CAS  PubMed  Google Scholar 

  • Kustan JM, Maruska KP, Fernald RD (2012) Subordinate male cichlids retain reproductive competence during social suppression. Proc R Soc Lond B 279:434–443

    Google Scholar 

  • Kustra MC, Alonzo SH (2020) Sperm and alternative reproductive tactics: a review of existing theory and empirical data. Philos Trans R Soc B 375:20200075

    Google Scholar 

  • Lavoie MD, Tedeschi JN, Garcia-Gonzalez F, Firman RC (2019) Exposure to male-dominated environments during development influences sperm sex ratios at sexual maturity. Evol Lett 3:392–402

    PubMed  PubMed Central  Google Scholar 

  • Lehnert SJ, ButtS IAE, Flannery EW, Peters KM, Heath DD, Pitcher TE (2017) Effects of ovarian fluid and genetic differences on sperm performance and fertilization success of alternative reproductive tactics in Chinook salmon. J Evol Biol 30:1236–1245

    CAS  PubMed  Google Scholar 

  • Lemaître JF, Ramm SA, Hurst JL, Stockley P (2011) Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal. Proc R Soc Lond B 278:1171–1176. https://doi.org/10.1098/rspb.2010.1828

    Article  Google Scholar 

  • Lemaître J-F, Ramm SA, Hurst JL, Stockley P (2012) Sperm competition roles and ejaculate investment in a promiscuous mammal. J Evol Biol 25:1216–1225. https://doi.org/10.1111/j.1420-9101.2012.02511.x

    Article  PubMed  Google Scholar 

  • Lewis JA, Pitcher TE (2017) The effects of rival seminal plasma on sperm velocity in the alternative reproductive tactics of Chinook salmon. Theriogenology 92:24–29

    PubMed  Google Scholar 

  • Lewis Z, Wedell N (2009) Male moths reduce sperm investment in relatives. Anim Behav 77:1547–1550

    Google Scholar 

  • Liberti J, Baer B, Boomsma JJ (2018) Rival seminal fluid induces enhanced sperm motility in a polyandrous ant. BMC Evol Biol 18:28

    CAS  PubMed  PubMed Central  Google Scholar 

  • Linklater JR, Wertheim B, Wigby S, Chapman T (2007) Ejaculate depletion patterns evolve in response to experimental manipulation of sex ratio in Drosophila melanogaster. Evolution 61:2027–2034

    PubMed  Google Scholar 

  • Locatello L, Pilastro A, Deana R, Zarpellon A, Rasotto MB (2007) Variation pattern of sperm quality traits in two gobies with alternative mating tactics. Funct Ecol 21:975–981. https://doi.org/10.1111/j.1365-2435.2007.01314.x

    Article  Google Scholar 

  • Locatello L, Poli F, Rasotto MB (2013) Tactic-specific differences in seminal fluid influence sperm performance. Proc R Soc B 280:20122891

    PubMed  PubMed Central  Google Scholar 

  • Lung O, Wolfner MF (2001) Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem Mol Biol 31:543–551

    CAS  PubMed  Google Scholar 

  • Lüpold S, Pitnick S (2018) Sperm form and function: what do we know about the role of sexual selection? Reproduction 155:R229–R243

    PubMed  Google Scholar 

  • Lüpold S, Birkhead TR, Westneat DF (2012a) Seasonal variation in ejaculate traits of male red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 66:1607–1617

    Google Scholar 

  • Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM, Pitnick S (2012b) How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 22:1667–1672. https://doi.org/10.1016/j.cub.2012.06.059

    Article  CAS  PubMed  Google Scholar 

  • Lüpold S, Pitnick S, Berben KS, Blengini CS, Belote JM, Manier MK (2013) Female mediation of competitive fertilization success in Drosophila melanogaster. P Natl Acad Sci USA 110:10693–10698

    Google Scholar 

  • Macartney EL, Crean AJ, Bonduriansky R (2018) Epigenetic paternal effects as costly, condition-dependent traits. Heredity 121:248–256

    PubMed  PubMed Central  Google Scholar 

  • Macartney EL, Crean AJ, Nakagawa S, Bonduriansky R (2019) Effects of nutrient limitation on sperm and seminal fluid: a systematic review and metaanalysis. Biol Rev 94:1722–1739. https://doi.org/10.1111/brv.12524

    Article  PubMed  Google Scholar 

  • Magris M, Chimetto G, Rizzi S, Pilastro A (2018) Quick-change artists: male guppies pay no cost to repeatedly adjust their sexual strategies. Behav Ecol 29:1113–1123

    Google Scholar 

  • Magris M, Zanata I, Rizzi S, Cattelan S, Pilastro A (2020a) Trade-offs of strategic sperm adjustments and their consequences under phenotype-environment mismatches in guppies. Anim Behav 166:171–181

    Google Scholar 

  • Magris M, Chimetto G, Pilastro A (2020b) Strategic ejaculate adjustments and mismatches: are males paying sperm senescence costs? Ethol Ecol Evol 32:389–401

    Google Scholar 

  • Makiguchi Y, Torao M, Kojima T, Pitcher TE (2016) Reproductive investment patterns and comparison of sperm quality in the presence and absence of ovarian fluid in alternative reproductive tactics of masu salmon, Oncorhynchus masou. Theriogenology 86:2189-2193.e2. https://doi.org/10.1016/j.theriogenology.2016.07.009

    Article  PubMed  Google Scholar 

  • Manier MK, Belote JM, Berben KS et al (2010) Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328:354–357

    CAS  PubMed  Google Scholar 

  • Marentette JR, Fitzpatrick JL, Berger RG, Balshine S (2009) Multiple male reproductive morphs in the invasive round goby (Apollonia melanostoma). J Great Lakes Res 35:302–308. https://doi.org/10.1016/j.jglr.2009.01.009

    Article  Google Scholar 

  • Martin PA, Reimers TJ, Lodge JR, Dziuk PJ (1974) The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. Reproduction 29:251–258

    Google Scholar 

  • McNamara KB, Elgar MA, Jones TM (2010) Adult responses to larval population size in the almond moth, Cadra cautella. Ethology 116:39–46

    Google Scholar 

  • Miller JS, Bose APH, Fitzpatrick JL, Balshine S (2019) Sperm maturation and male tactic-specific differences in ejaculates in the plainfin midshipman fish Porichthys notatus. J Fish Biol 94:434–445. https://doi.org/10.1111/jfb.13912

    Article  PubMed  Google Scholar 

  • Moatt JP, Dytham C, Thom MDF (2014) Sperm production responds to perceived sperm competition risk in male Drosophila melanogaster. Physiol Behav 131:111–114. https://doi.org/10.1016/j.physbeh.2014.04.027

    Article  CAS  PubMed  Google Scholar 

  • Mohorianu I, Bretman A, Smith DT, Mohorianu I, Bretman A, Smith DT, Fowler EK, Dalmay T, Chapman T (2017) Genomic responses to the socio-sexual environment in male Drosophila melanogaster exposed to conspecific rivals. RNA 23:1048–1059

    CAS  PubMed  PubMed Central  Google Scholar 

  • Montrose TV, Harris EW, Moore AJ, Moore PJ (2008) Sperm competition within a dominance hierarchy: investment in social status vs. investment in ejaculates. J Evol Biol 21:1290–1296. https://doi.org/10.1111/j.1420-9101.2008.01570.x

    Article  Google Scholar 

  • Morrow EH, Leijon A, Meerupati A (2008) Hemiclonal analysis reveals significant genetic, environmental and genotype x environment effects on sperm size in Drosophila melanogaster. J Evol Biol 21:1692–1702. https://doi.org/10.1111/j.1420-9101.2008.01585.x

    Article  CAS  PubMed  Google Scholar 

  • Moschilla JA, Tomkins JL, Simmons LW (2020) Males adjust their manipulation of female remating in response to sperm competition risk. Proc R Soc B 287:20201238

    PubMed  Google Scholar 

  • Nakadera Y, Giannakara A, Ramm SA (2019) Plastic expression of seminal fluid protein genes in a simultaneously hermaphroditic snail. Behav Ecol 30:904–913. https://doi.org/10.1093/beheco/arz027

    Article  Google Scholar 

  • Nakanishi A, Takegaki T (2019) Tactic-specific sperm traits in the dusky frillgoby (Bathygobius fuscus). J Zool 307:71–77

    Google Scholar 

  • Neff BD, Fu P, Gross MR (2003) Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behav Ecol 14:634–641

    Google Scholar 

  • Nguyen TTX, Moehring AJ (2018) A male’s seminal fluid increases later competitors’ productivity. J Evol Biol 31:1572–1581. https://doi.org/10.1111/jeb.13352

    Article  PubMed  Google Scholar 

  • Oppliger A, Hosken DJ, Ribi G (1998) Snail sperm production characteristics vary with sperm competition risk. Proc R Soc Lond B 265:1527–1534

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567. https://doi.org/10.1111/j.1469-185X.1970.tb01176.x

    Article  Google Scholar 

  • Parker GA (1990a) Sperm competition games—raffles and roles. Proc R Soc Lond B 242:120–126. 10. 1098/rspb.1990.0114

  • Parker GA (1990b) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Lond B 242:127–133

    Google Scholar 

  • Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc Lond B 253:245–254. https://doi.org/10.1098/rspb.1993.0110

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934. https://doi.org/10.1111/j.1469-185X.2010.00140.x

    Article  PubMed  Google Scholar 

  • Parker GA, Ball MA, Stockley P, Gage MJG (1996) Sperm competition games: Individual assessment of sperm competition intensity by group spawners. Proc R Soc Lond B 263:1291–1297. https://doi.org/10.1098/rspb.1996.0189

    Article  Google Scholar 

  • Parker GA, Immler S, Pitnick S, Birkhead TR (2010) Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. J Theor Biol 264:1003–1023

    CAS  PubMed  Google Scholar 

  • Patlar B, Ramm SA (2020) Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability. J Evol Biol 33:225–236. https://doi.org/10.1111/jeb.13568

    Article  PubMed  Google Scholar 

  • Patlar B, Weber M, Ramm SA (2018) Genetic and environmental variation in transcriptional expression of seminal fluid proteins. Heredity 122:595–611

    PubMed  PubMed Central  Google Scholar 

  • Peretti AV, Eberhard WG (2010) Cryptic female choice via sperm dumping favours male copulatory courtship in a spider. J Evol Biol 23:271–281

    CAS  PubMed  Google Scholar 

  • Perry JC, Rowe L (2010) Condition-dependent ejaculate size and composition in a ladybird beetle. Proc R Soc Lond B 277:3639–3647. https://doi.org/10.1098/rspb.2010.0810

    Article  Google Scholar 

  • Perry JC, Sirot L, Wigby S (2013) The seminal symphony: how to compose an ejaculate. Trends Ecol Evol 28:414–422

    PubMed  PubMed Central  Google Scholar 

  • Pilastro A, Evans JP, Sartorelli S, Bisazza A (2002) Male phenotype predicts insemination success in guppies. 269:1325–1330. https://doi.org/10.1098/rspb.2002.2017

  • Pilastro A, Simonato M, Bisazza A, Evans JP (2004) Cryptic female preference for colorful males in guppies. Evolution 58:665–669

    PubMed  Google Scholar 

  • Pilastro A, Mandelli M, Gasparini C, Dadda M, Bisazza A (2007) Copulation duration, insemination efficiency and male attractiveness in guppies. Anim Behav 74:321–328. https://doi.org/10.1016/j.anbehav.2006.09.016

    Article  Google Scholar 

  • Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, London, pp 69–149

    Google Scholar 

  • Pizzari T, Birkhead TR (2000) Female feral fowl eject sperm of subdominant males. Nature 405:787–789

    CAS  PubMed  Google Scholar 

  • Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, London, pp 207–245

    Google Scholar 

  • Pizzari T, Cornwallis CK, Løvlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74

    CAS  PubMed  Google Scholar 

  • Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310. https://doi.org/10.1007/s00265-006-0178-0

    Article  Google Scholar 

  • Poli F, Locatello L, Rasotto MB (2018) Seminal fluid enhances competitiveness of territorial males’ sperm in a fish with alternative male reproductive tactics. J Exp Biol 221:jeb175976. https://doi.org/10.1242/jeb.175976

  • Pound N (1999) Effects of morphine on electrically evoked contractions of the vas deferens in two congeneric rodent species differing in sperm competition intensity. Proc R Soc Lond B 266:1755–1758

    CAS  Google Scholar 

  • Price TA, Lizé A, Marcello M, Bretman A (2012) Experience of mating rivals causes males to modulate sperm transfer in the fly Drosophila pseudoobscura. J Insect Physiol 58:1669–1675

    CAS  PubMed  Google Scholar 

  • Ram KR, Wolfner MF (2007) Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet 3:e238

    PubMed  PubMed Central  Google Scholar 

  • Ramm SA (2020) Seminal fluid and accessory male investment in sperm competition. Phil Trans R Soc B Biol Sci 375:20200068

    Google Scholar 

  • Ramm SA, Stockley P (2009) Male house mice do not adjust sperm allocation in response to odours from related or unrelated rivals. Anim Behav 78:685–690

    Google Scholar 

  • Ramm SA, Edward DA, Claydon AJ, Hammond DE, Brownridge P, Hurst JL, Beynon RJ, Stockley P (2015) Sperm competition risk drives plasticity in seminal fluid composition. BMC Biol 13:87. https://doi.org/10.1186/s12915-015-0197-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramm SA, Lengerer B, Arbore R, Pjeta R, Wunderer J, Giannakara A, Berezikov E, Ladurner P, Schärer L (2019) Sex allocation plasticity on a transcriptome scale: socially sensitive gene expression in a simultaneous hermaphrodite. Mol Ecol 28:2321–2341. https://doi.org/10.1111/mec.15077

    Article  CAS  PubMed  Google Scholar 

  • Rasotto MB (2002) Male traits associated with alternative reproductive tactics in Gobius niger. J Fish Biol 61:173–184. https://doi.org/10.1006/jfbi.2002.2029

    Article  Google Scholar 

  • Rasotto MB, Shapiro DY (1998) Morphology of gonoducts and male genital papilla, in the bluehead wrasse: implications and correlates on the control of gamete release. J Fish Biol 52:716–725

    Google Scholar 

  • Reinhardt K (2007) Evolutionary consequences of sperm cell aging. Q Rev Biol 82:375–393

    PubMed  Google Scholar 

  • Reinhardt K, Naylor R, Siva-Jothy MT (2011) Male mating rate is constrained by seminal fluid availability in bedbugs, Cimex lectularius. PLoS ONE 6:e22082

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhold K, Kurtz J, Engqvist L (2002) Cryptic male choice: sperm allocation strategies when female quality varies. J Evol Biol 15:201–209

    Google Scholar 

  • Rojas Mora A, Meniri M, Gning O, Glauser G, Vallat A, Helfenstein F (2017) Antioxidant allocation modulates sperm quality across changing social environments. PLoS ONE 12:e0176385. https://doi.org/10.1371/journal.pone.0176385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rudolfsen G, Figenschou L, Folstad I, Tveiten H, Figenschou M (2006) Rapid adjustments of sperm characteristics in relation to social status. Proc R Soc Lond B 273:325–332. https://doi.org/10.1098/rspb.2005.3305

    Article  Google Scholar 

  • Sakaluk SK, Müller JK (2008) Risk of sperm competition mediates copulation duration, but not paternity, of male burying beetles. J Insect Behav 21:153–163

    Google Scholar 

  • Schärer L, Vizoso DB (2007) Phenotypic plasticity in sperm production rate: there’s more to it than testis size. Evol Ecol 21:295–306

    Google Scholar 

  • Schrempf A, Moser A, Delabie J, Heinze J (2016) Sperm traits differ between winged and wingless males of the ant Cardiocondyla obscurior. Integr Zool 11:427–432. https://doi.org/10.1111/1749-4877.12191

    Article  PubMed  Google Scholar 

  • Schulte-Hostedde AI, Burness G (2005) Fertilization dynamics of sperm from different male mating tactics in bluegill (Lepomis macrochirus). Can J Zool 83:1638–1642

    Google Scholar 

  • Sekii K, Vizoso DB, Kuales G, De Mulder K, Ladurner P, Schärer L (2013) Phenotypic engineering of sperm-production rate confirms evolutionary predictions of sperm competition theory. Proc R Soc B 280:20122711

    PubMed  PubMed Central  Google Scholar 

  • Shapiro DY, Marconato A, Yoshikawa T (1994) Sperm Economy in a Coral Reef Fish, Thalassoma Bifasciatum. Ecology 75:1334–1344

    Google Scholar 

  • Silberglied RE, Shepherd JG, Dickinson JL (1984) Eunuchs: the role of apyrene sperm in Lepidoptera? Am Nat:255–265

  • Silva WTAF, Sáez-Espinosa P, Torijo-Boix S, Romero A, Devaux C, Durieux M, Gómez-Torres MJ, Immler S (2019) The effects of male social environment on sperm phenotype and genome integrity. J Evol Biol 32:535–544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

    Google Scholar 

  • Simmons LW (2011) Resource allocation trade-off between sperm quality and immunity in the field cricket, Teleogryllus oceanicus. Behav Ecol 23:168–173. https://doi.org/10.1093/beheco/arr170

    Article  Google Scholar 

  • Simmons LW, Beveridge M (2011) Seminal fluid affects sperm viability in a cricket. PLoS ONE 6:e17975. https://doi.org/10.1371/journal.pone.0017975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simmons LW, Fitzpatrick JL (2012) Sperm wars and the evolution of male fertility. Reproduction 144:519–534

    CAS  PubMed  Google Scholar 

  • Simmons LW, Kotiaho JS (2007) Quantitative genetic correlation between trait and preference supports a sexually selected sperm process. P Natl Acad Sci USA 104:16604–16608

    CAS  Google Scholar 

  • Simmons LW, Kvarnemo C (1997) Ejaculate expenditure by malebush crickets decreases with sperm competition intensity. Phil Trans R Soc B Biol Sci 264:1203–1208

    Google Scholar 

  • Simmons LW, Lovegrove M (2017) Socially cued seminal fluid gene expression mediates responses in ejaculate quality to sperm competition risk. Proc R Soc B 284:20171486

    PubMed  PubMed Central  Google Scholar 

  • Simmons LW, Moore AJ (2009) Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, London, pp 405–434

    Google Scholar 

  • Simmons LW, Craig M, Llorens T, Schinzig M, Hosken D (1993) Bushcricket spermatophores vary in accord with sperm competition and parental investment theory. Proc R Soc Lond B 251:183–186

    Google Scholar 

  • Simmons LW, Tomkins JL, Hunt J (1999) Sperm competition games played by dimorphic male beetles. Proc R Soc Lond B 266:145–150

    Google Scholar 

  • Simmons LW, Denholm A, Jackson C, Levy E, Madon E (2007) Male crickets adjust ejaculate quality with both risk and intensity of sperm competition. Biol Lett 3:520–522. https://doi.org/10.1098/rsbl.2007.0328

    Article  PubMed  PubMed Central  Google Scholar 

  • Simmons LW, Lüpold S, Fitzpatrick JL (2017) Evolutionary trade-off between secondary sexual traits and ejaculates. Trends Ecol Evol 32:964–976

    PubMed  Google Scholar 

  • Sirot LK (2019) Modulation of seminal fluid molecules by males and females. Curr Opin Insect Sci 35:109–116

    PubMed  Google Scholar 

  • Sirot LK, Wolfner MF, Wigby S (2011) Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. P Natl Acad Sci USA 108:9922–9926. https://doi.org/10.1073/pnas.1100905108

    Article  Google Scholar 

  • Sloan NS, Lovegrove M, Simmons LW (2018) Social manipulation of sperm competition intensity reduces seminal fluid gene expression. Biol Lett 14:20170659

    PubMed  PubMed Central  Google Scholar 

  • Smith CC (2012) Opposing effects of sperm viability and velocity on the outcome of sperm competition. Behav Ecol 23:820–826

    Google Scholar 

  • Smith CC, Ryan MJ (2010) Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J Evol Biol 23:1759–1771. https://doi.org/10.1111/j.1420-9101.2010.02041.x

    Article  CAS  PubMed  Google Scholar 

  • Smith CC, Ryan MJ (2011) Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis. Biol Lett 7:733–735

    PubMed  PubMed Central  Google Scholar 

  • Smith C, Pateman-Jones C, Zięba G, Przybylski M, Reichard M (2009) Sperm depletion as a consequence of increased sperm competition risk in the European bitterling, Rhodeus amarus. Anim Behav 77:1227–1233

    Google Scholar 

  • Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53. https://doi.org/10.1016/j.tree.2004.10.011

    Article  PubMed  Google Scholar 

  • Soubry A, Hoyo C, Jirtle RL, Murphy SK (2014) A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. Bioessays 36:359–371

    CAS  PubMed  PubMed Central  Google Scholar 

  • Spagopoulou F, Vega-Trejo R, Head ML, Jennions MD (2020) Shifts in reproductive investment in response to competitors lower male reproductive success. Am Nat 196:355–368

    PubMed  Google Scholar 

  • Stoltz JA, Neff BD (2006) Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J Evol Biol 19:1873–1881. https://doi.org/10.1111/j.1420-9101.2006.01165.x

    Article  CAS  PubMed  Google Scholar 

  • Stouder C, Paoloni-Giacobino A (2010) Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 139:373–379

    CAS  PubMed  Google Scholar 

  • Suarez SS (2016) Mammalian sperm interactions with the female reproductive tract. Cell Tissue Res 363:185–194. https://doi.org/10.1007/s00441-015-2244-2

    Article  PubMed  Google Scholar 

  • Sutter A, Immler S (2020) Within-ejaculate sperm competition. Philos Trans R Soc B 375:20200066

    CAS  Google Scholar 

  • Taborsky M (1998) Sperm competition in fish: ’bourgeois’ males and parasitic spawning. Trends Ecol Evol 13:222–227

    CAS  PubMed  Google Scholar 

  • Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86:1–13

    PubMed  Google Scholar 

  • Thomas ML, Simmons LW (2007) Male crickets adjust the viability of their sperm in response to female mating status. Am Nat 170:190–195. https://doi.org/10.1086/519404

    Article  PubMed  Google Scholar 

  • Thomas ML, Simmons LW (2009a) Male dominance influences pheromone expression, ejaculate quality, and fertilization success in the Australian field cricket, Teleogryllus oceanicus. Behav Ecol 20:1118–1124. https://doi.org/10.1093/beheco/arp105

    Article  Google Scholar 

  • Thomas ML, Simmons LW (2009b) Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets. Proc R Soc Lond B 276:383–388. https://doi.org/10.1098/rspb.2008.1206

    Article  Google Scholar 

  • Thorburn D-MJ, Knell RJ, Parrett JM (2018) Sperm morph and remating frequency in the Indian meal moth, Plodia interpunctella. Biol Lett 14:20180304

    PubMed  PubMed Central  Google Scholar 

  • Todd EV, Liu H, Lamm MS, Thomas JT, Rutherford K, Thompson KC, Godwin JR, Gemmell NJ (2018) Female mimicry by sneaker males has a transcriptomic signature in both the brain and the gonad in a sex-changing fish. Mol Biol Evol 35:225–241. https://doi.org/10.1093/molbev/msx293

    Article  CAS  PubMed  Google Scholar 

  • Tomislav V. Vladić, Torbjörn Järvi, (2001) Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proceedings of the Royal Society of London. Series B: Biological Sciences 268 (1483):2375-2381

  • Tuni C, Perdigón Ferreira J, Fritz Y, Meneses AM, Gasparini C (2016) Impaired sperm quality, delayed mating but no costs for offspring fitness in crickets winning a fight. J Evol Biol 29:1643–1647

    CAS  PubMed  Google Scholar 

  • Turnell BR, Shaw KL, Reeve HK (2018) Modeling strategic sperm allocation: tailoring the predictions to the species. Evolution 72:414–425

    PubMed  Google Scholar 

  • Uglem I, Galloway T, Rosenqvist G, Folstad I (2001) Male dimorphism, sperm traits and immunology in the corkwing wrasse (Symphodus melops L.). Behav Ecol Sociobiol 50:511–518

    Google Scholar 

  • Uglem I, Mayer I, Rosenqvist G (2002) Variation in plasma steroids and reproductive traits in dimorphic males of corkwing wrasse (Symphodus melops L.). Horm Behav 41:396–404. https://doi.org/10.1006/hbeh.2002.1779

    Article  CAS  PubMed  Google Scholar 

  • Van Voorhies WA (1992) Production of sperm reduces nematode lifespan. Nature 360:456–458

    PubMed  Google Scholar 

  • Vaz Serrano J, Folstad I, Rudolfsen G, Figenschou L (2006) Do the fastest sperm within an ejaculate swim faster in subordinate than in dominant males of Arctic char? Can J Zool 84:1019–1024

    Google Scholar 

  • Vermeulen A, Engels S, Engqvist L, Sauer KP (2009) Phenotypic plasticity in sperm traits in scorpionflies (Mecoptera: Panorpidae): consequences of larval history and seasonality on sperm length and sperm transfer. Eur J Entomol 106:347–352

    Google Scholar 

  • Villagrán M, Ungerfeld R (2013) Permanent contact with females increases testosterone and improves fresh semen traits in pampas deer (Ozotoceros bezoarticus) males. Anim Reprod Sci 143:85–90. https://doi.org/10.1016/j.anireprosci.2013.10.011

    Article  CAS  PubMed  Google Scholar 

  • Vladić TV (2000) The effect of water temperature on sperm motility of adult male and precocious male parr of Atlantic salmon and brown trout. Int Ver The 27:1070–1074

    Google Scholar 

  • Vladić T, Forsberg LA, Järvi T (2010) Sperm competition between alternative reproductive tactics of the Atlantic salmon in vitro. Aquaculture 302:265–269

    Google Scholar 

  • Warner RR, Shapiro DY, Marcanato A, Petersen CW (1995) Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females. Proc R Soc Lond B 262:135–139

    CAS  Google Scholar 

  • Wedell N, Cook PA (1999a) Strategic sperm allocation in the Small White butterfly Pieris rapae (Lepidoptera: Pieridae). Funct Ecol 13:85–93. https://doi.org/10.1046/j.1365-2435.1999.00286.x

    Article  Google Scholar 

  • Wedell N, Cook PA (1999b) Butterflies tailor their ejaculate in response to sperm competition risk and intensity. Proc R Soc Lond B 266:1033–1039

    Google Scholar 

  • Wedell N, Ritchie MG (2004) Male age, mating status and nuptial gift quality in a bushcricket. Anim Behav 67:1059–1065

    Google Scholar 

  • Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320. https://doi.org/10.1016/S0169-5347(02)02533-8

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Whitman DW, Agrawal AA (2009) What is phenotypic plasticity and why is it important. In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science Publishers, Enfield, pp 1–63

    Google Scholar 

  • Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, Wolfner MF, Chapman T (2009) Seminal fluid protein allocation and male reproductive success. Curr Biol 19:751–757. https://doi.org/10.1016/j.cub.2009.03.036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wigby S, Perry JC, Kim YH, Sirot LK (2015) Developmental environment mediates male seminal protein investment in Drosophila melanogaster. Funct Ecol 30:410–419

    PubMed  PubMed Central  Google Scholar 

  • Wigby S, Brown NC, Allen SE, Misra S, Sitnik JL, Sepil I, Clark AG, Wolfner MF (2020) The Drosophila seminal proteome and its role in postcopulatory sexual selection. Philos Trans R Soc B 375:20200072. https://doi.org/10.1098/rstb.2020.0072

    Article  CAS  Google Scholar 

  • Zajitschek S, Hotzy C, Zajitschek F, Immler S (2014) Short-term variation in sperm competition causes sperm-mediated epigenetic effects on early offspring performance in the zebrafish. Proc R Soc B 281:20140422

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I thank Andrea Pilastro for giving me the opportunity to write this review and for his suggestions and support along the way. I am grateful to Cristina Tuni for her precious feedback, to Steven Ramm for valuable comments, and to Giuseppe Fusco and Mariella Rasotto for fruitful discussion about phenotypic plasticity. I also thank three anonymous referees for their useful comments on previous versions of the manuscript.

Funding

This work was supported by a PhD fellowship from the University of Padova to MM.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martina Magris.

Ethics declarations

Conflict of interest

The author declares to have no conflict of interest.

Additional information

Communicated by F. Trillmich

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Magris, M. Strategic adjustment of ejaculate quality in response to variation of the socio-sexual environment. Behav Ecol Sociobiol 75, 91 (2021). https://doi.org/10.1007/s00265-021-03032-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-021-03032-1

Keywords

Navigation