Evolutionary Ecology

, Volume 33, Issue 2, pp 149–172 | Cite as

Males can evolve lower resistance to sexually transmitted infections to infect their mates and thereby increase their own fitness

  • Sophie Johns
  • Jonathan M. HenshawEmail author
  • Michael D. Jennions
  • Megan L. Head
Original Paper


Sexually transmitted infections (STIs) often lower their host’s future reproductive success by inducing sterility. Females can minimise the reproductive cost of infection by plastically increasing their current reproductive effort (i.e. terminal investment) before they become sterile. In polyandrous systems, long-term female survival or fecundity is often irrelevant to male fitness. Mating with an infected, terminally investing female potentially yields greater fitness gains for males than mating with an uninfected female. Males might consequently benefit from infecting females with an STI. We construct mathematical models of the evolutionary consequences of a sterilising STI. We show that females should terminally invest in response to an STI when immune investment is relatively ineffective at delaying STI-induced sterility. Cost-effective immune responses may conversely select for reduced reproductive effort after infection (‘terminal divestment’). Crucially, we then show that female terminal investment can select for lower STI resistance in males. This selection is driven by fitness gains to males that acquire the STI and subsequently infect their mates, which offset any costs of infection (e.g. male sterility). This type of adaptive mate harm generates sexual conflict over the optimal level of resistance to STIs. It could partly explain why immune reactions to new infections are weaker in males than females of many species.


Life history Model Sexual conflict Sexual dimorphism Sexually antagonistic Terminal investment 



Funding was provided by Australian Research Council (Grant No. FT160100149).

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.


  1. Altincicek B, Gross J, Vilcinskas A (2008) Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 17(6):711–716Google Scholar
  2. Amininasab SM, Birker M, Kingma SA, Hildenbrandt H, Komdeur J (2017) The effect of male incubation feeding on female nest attendance and reproductive performance in a socially monogamous bird. J Ornithol 158(3):687–696Google Scholar
  3. Antonovics J, Boots M, Abbate J, Baker C, McFrederick Q, Panjeti V (2011) Biology and evolution of sexual transmission. Ann N Y Acad Sci 1230:12–24Google Scholar
  4. Armitage SAO, Thompson JJW, Rolff J, Siva-Jothy MT (2003) Examining costs of induced and constitutive immune investment in Tenebrio molitor. J Evol Biol 16(5):1038–1044Google Scholar
  5. Ashby B, Gupta S (2013) Sexually transmitted infections in polygamous mating systems. Philos Trans R Soc B 368(1613):20120048Google Scholar
  6. Bonduriansky R (2014) The ecology of sexual conflict: background mortality can modulate the effects of male manipulation on female fitness. Evolution 68(2):595–604Google Scholar
  7. Bonneaud C, Mazuc J, Chastel O, Westerdahl H, Sorci G (2004) Terminal investment induced by immune challenge and associated with major histocompatibility complex in the house sparrow. Evolution 58(12):2823–2830Google Scholar
  8. Booksmythe I, Mautz B, Davis J, Nakagawa S, Jennions MD (2017) Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta-analysis. Biol Rev 92(1):108–134Google Scholar
  9. Bowers EK, Smith RA, Hodges CJ, Zimmerman LM, Thompson CF, Sakaluk SK (2012) Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon). Proc R Soc B 279(1739):2891–2898Google Scholar
  10. Bowers EK, Bowden RM, Sakaluk SK, Thompson CF (2015) Immune activation generates corticosterone-mediated terminal reproductive investment in a wild bird. Am Nat 185(6):769–783Google Scholar
  11. Brown GP, Shilton CM, Shine R (2011) Measuring amphibian immunocompetence: validation of the phytohemagglutinin skin-swelling assay in the cane toad, Rhinella marina. Methods Ecol Evol 2:341–348Google Scholar
  12. Chapman T, Miyatake T, Smith HK, Partidge L (1998) Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc R Soc B 265(1408):1879–1894Google Scholar
  13. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18(1):41–47Google Scholar
  14. Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123(2):212–229Google Scholar
  15. Cordoba-Aguilar A, Contreras-Garduno J, Peralta-Vazquez H, Luna-Gonzalez A, Campa-Cordova AI, Ascencio F (2006) Sexual comparisons in immune ability, survival and parasite intensity in two damselfly species. J Insect Physiol 52(8):861–869Google Scholar
  16. Courchamp F, Clutton-Brock T, Greenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410Google Scholar
  17. Cousineau SV, Alizon S (2014) Parasite evolution in response to sex-based host heterogeneity in resistance and tolerance. J Evol Biol 27:2753–2766Google Scholar
  18. Creighton JC, Heflin ND, Belk MC (2009) Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am Nat 174(5):673–684Google Scholar
  19. Duffield KR, Bowers EK, Sakaluk SK, Sadd BM (2017) A dynamic threshold model for terminal investment. Behav Ecol Sociobiol 71(12):185Google Scholar
  20. Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, Vignat J, Ferlay J, Bray F, Plummer M, Franceschi S (2012) Global burden of human papillomavirus and related diseases. Vaccine 30(Suppl. 5):F12–F23Google Scholar
  21. Giehr J, Grasse AV, Cremer S, Heinze J, Schrempf A (2017) Ant queens increase their reproductive efforts after pathogen infection. R Soc Open Sci 4(7):28791176Google Scholar
  22. Gimenes F, Souza RP, Bento JC, Teixeira JJV, Maria-Engler SS, Bonini MG, Consolaro MEL (2014) Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol 11(12):672–687Google Scholar
  23. Gipson SAY, Hall MD (2016) The evolution of sexual dimorphism and its potential impact on host-pathogen coevolution. Evolution 70:959–968Google Scholar
  24. Grossman C (1989) Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. J Steroid Biochem 34(1–6):241–251Google Scholar
  25. Haaland TR, Wright J, Kuijper B, Ratikainen II (2017) Differential allocation revisited: when should mate quality affect parental investment? Am Nat 190(4):534–546Google Scholar
  26. Hanssen SA (2006) Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87(10):2440–2446Google Scholar
  27. Hansen M, Flatt T, Aguilaniu H (2013) Reproduction, fat metabolism, and life span: what is the connection? Cell Metab 17(1):10–19Google Scholar
  28. Holman L, Kokko H (2013) The consequences of polyandry for population viability, extinction risk and conservation. Philos Trans R Soc B 368(1613):20120053Google Scholar
  29. Hosken DJ (2001) Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies. Curr Biol 11:R379–R380Google Scholar
  30. Houston AI, McNamara JM (2005) John Maynard Smith and the importance of consistency in evolution game theory. Biol Philos 20:933–950Google Scholar
  31. Hurst GDD, Sharpe RG, Broomfield AH, Walker LE, Majerus TMO, Zakharov IA, Majerus MEN (1995) Sexually transmitted disease in promiscuous insect, Adalia bipunctata. Ecol Entomol 20(3):230–236Google Scholar
  32. Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc B 267:665–670Google Scholar
  33. Jennions MD, Fromhage L (2017) Not all sex ratios are equal: the Fisher condition, parental care and sexual selection. Philos Trans R Soc B 372(1729):20160312Google Scholar
  34. Johnstone RA, Keller L (2000) How males can gain by harming their mates: sexual conflict, seminal toxins, and the cost of mating. Am Nat 156(4):368–377Google Scholar
  35. Keller IS, Bayer T, Salzburger W, Roth O (2018) Effects of parental care on resource allocation into immune defense and buccal microbiota in mouthbrooding cichlid fishes. Evolution 72(5):1109–1123Google Scholar
  36. Kelly CD, Stoehr AM, Nunn C, Smyth KN, Prokop ZM (2018) Sexual dimorphism in immunity across animals: a meta-analysis. Ecol Lett. Google Scholar
  37. Knell RJ, Webberley KM (2004) Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour. Biol Rev 79(3):557–581Google Scholar
  38. Krams I, Burghardt GM, Krams R, Trakimas G, Kaasik A, Luoto S, Rantala MJ, Krama T (2016) A dark cuticle allows higher investment in immunity, longevity and fecundity in a beetle upon a simulated parasite attack. Oecologia 182(1):99–109Google Scholar
  39. Kruuk H, Parish T (1982) Factors affecting population density, group size and territory size of the European badger, Meles meles. J Zool 196(1):31–39Google Scholar
  40. Lack D (1947) The significance of clutch-size. Ibis 89:302–352Google Scholar
  41. Lessells CM (2005) Why are males bad for females? Models for the evolution of damaging male mating behavior. Am Nat 165(5):S46–S63Google Scholar
  42. Lockhart AB, Thrall PH, Antonovics J (1996) Sexually transmitted diseases in animals: ecological and evolutionary implications. Biol Rev 71:415–471Google Scholar
  43. Marriott I, Huet-Hudson YM (2006) Sexual dimorphism in innate immune responses to infectious organisms. Immunol Res 34(3):177–192Google Scholar
  44. McLeod DV, Day T (2017) Female plasticity tends to reduce sexual conflict. Nat Ecol Evol 1:0054Google Scholar
  45. McNamara KB, Simmons LW (2017) Experimental evolution reveals differences between phenotypic and evolutionary responses to population density. J Evol Biol 30(9):1763–1771Google Scholar
  46. Morrow EH, Arnqvist G, Pitnick S (2003) Adaptation versus pleiotropy: why do males harm their mates? Behav Ecol 14(6):802–806Google Scholar
  47. Nandy B, Gupta V, Udaykumar N, Samant MA, Sen S, Prasad NG (2013) Experimental evolution of female traits under different levels of intersexual conflict in Drosophila melanogaster. Evolution 68(2):412–425Google Scholar
  48. Norris K (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26Google Scholar
  49. Pennell TM, Morrow EH (2013) Two sexes, one genome: the evolutionary dynamics of intralocus sexual conflict. Ecol Evol 3(6):1819–1834Google Scholar
  50. Perry JC, Rowe L (2015) The evolution of sexually antagonistic phenotypes. Cold Spring Harbor Perspect Biol 7(6):a017558Google Scholar
  51. Reaney LT, Knell RJ (2010) Immune activation but not male quality affects female current reproductive investment in a dung beetle. Behav Ecol 21(6):1367–1372Google Scholar
  52. Reavey CE, Warnock ND, Vogel H, Cotter SC (2014) Trade-offs between personal immunity and reproduction in the burying beetle, Nicrophorus vespilloides. Behav Ecol 25(2):415–423Google Scholar
  53. Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381(6579):232–234Google Scholar
  54. Rittschof CC, Pattanaik S, Johnson L, Matos LF, Brusini J, Wayne ML (2013) Sigma virus and male reproductive success in Drosophila melanogaster. Behav Ecol Sociobiol 67(4):529–540Google Scholar
  55. Rolff J (2002) Bateman’s principle and immunity. Proc R Soc B 269(1493):867–872Google Scholar
  56. Rolff J, Armitage SAO, Coltman DW (2005) Genetic constraints and sexual dimorphism in immune defense. Evolution 59(8):1844–1850Google Scholar
  57. Ruiz-Guzmán G, Ramos-Castaneda J, Hernandez-Quintero A, Contreras-Garduno J (2016) Costs and benefits of vertical and horizontal transmission of dengue virus. J Exp Biol 219(Pt 22):3665–3669Google Scholar
  58. Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116(12):2017–2026Google Scholar
  59. Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction-immunity trade-offs in insects. Annu Rev Entomol 61:239–256Google Scholar
  60. Simmons AM, Rodgers CE (1994) Effect of an ectoparasitic nematode, Noctuidonema guyanense, on adult longevity and egg fertility in Spodoptera frugiperda (lepidoptera, noctuidae). Biol Control 4(3):285–289Google Scholar
  61. Snook RR, Markow TA (2002) Efficiency of gamete usage in nature: sperm storage, fertilization and polyspermy. Proc R Soc B 269(1490):467–473Google Scholar
  62. Staudacher H, Menken SBJ, Groot AT (2015) Effects of immune challenge on the oviposition strategy of a noctuid moth. J Evol Biol 28(8):1568–1577Google Scholar
  63. Stearns SC (1976) Life-history tactics—review of ideas. Q Rev Biol 51(1):3–47Google Scholar
  64. Strandberg JO, Tucker LC (1974) Filariomyces forficulae: occurrence and effects on predatory earwig, Labidura riparia. J Invertebr Pathol 24(3):357–364Google Scholar
  65. Sylvestre G, Gandini M, Maciel-de-Freitas R (2013) Age-dependent effects of oral infection with dengue virus on Aedes aegypti (Diptera: Culicidae) feeding behavior, survival, oviposition success and fecundity. PLoS ONE 8(3):e59933Google Scholar
  66. Taylor PD (1996) The selection differential in quantitative genetic and ESS models. Evolution 50(5):2106–2110Google Scholar
  67. Thrall PH, Antonovics J, Hall DW (1993) Host and pathogen coexistence in sexually transmitted and vector-borne diseases characterized by frequency-dependent disease transmission. Am Nat 142(3):543–552Google Scholar
  68. Thrall PH, Antonovics J, Dobson AP (2000) Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proc R Soc B 267(1452):1555–1563Google Scholar
  69. Travers LM, Garcia-Gonzalez F, Simmons LW (2015) Live fast die young life history in females: evolutionary trade-off between early life mating and lifespan in female Drosophila melanogaster. Sci Rep 5:15469Google Scholar
  70. Tschirren B, Fitze PS, Richner H (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Am Ecol 72(5):839–845Google Scholar
  71. Tyson R, Haines S, Hodges KE (2010) Modelling the Canada lynx and snowshoe hare population cycle: the role of specialist predators. Theor Ecol 3(2):97–111Google Scholar
  72. Úbeda F, Jansen VAA (2016) The evolution of sex-specific virulence in infectious diseases. Nat Commun 7:13849Google Scholar
  73. Vézilier J, Nicot A, Gandon S, Rivero A (2012) Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proc R Soc B 279(1744):4033–4041Google Scholar
  74. Vincent CM, Sharp NP (2014) Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster. Proc Biol Sci B 281(1788):20140987Google Scholar
  75. Webberley KM, Hurst GDD, Husband RW, Schulenburg HGVD, Sloggett JJ, Isham V, Buszko J, Majerus MEN (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution and coccinellid beetles. J Am Ecol 73(1):1–10Google Scholar
  76. Wigby S, Chapman T (2004) Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58(5):1028–1037Google Scholar
  77. Wilburn DB, Swanson WJ (2016) From molecules to mating: rapid evolution and biochemical studies of reproduction proteins. J Proteom 135:12–25Google Scholar
  78. Williams GC (1966) Natural selection costs of reproduction and a refinement of Lack’s principle. Am Nat 100(916):687–690Google Scholar
  79. Wolfner MF (1997) Tokens of love: functions and regulation of drosophila male accessory gland products. Insect Biochem Mol 27(3):179–192Google Scholar
  80. Wolfner MF (2002) The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88(2):85–93Google Scholar
  81. Yapici N, Kim Y-J, Ribeiro C, Dickson BJ (2008) A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451(7174):33–37Google Scholar
  82. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26(10):1009–1023Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Division of Ecology and Evolution, Research School of BiologyThe Australian National UniversityCanberraAustralia
  2. 2.Department of Biological SciencesUniversity of IdahoMoscowUSA

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