Advertisement

Polyandrous mating increases offspring production and lifespan in female Drosophila arizonae

  • Dean A. Croshaw
  • Marisol Gómez
Original Article

Abstract

Multiple mating by females is a widespread but often costly behavior. However, according to the Bateman principle, mating with multiple males may not increase the number of offspring produced by females. Despite the Bateman paradigm, many studies have shown advantages to polyandry. We investigated the fitness consequences of different mating regimes (virginity, once-mated, serial monogamy, and polyandry) in Drosophila arizonae, a species in which females remate frequently, experience a possible cost of mating in the form of an insemination reaction, and receive nutritive seminal contributions from males. Although monogamous and polyandrous females mated at similar rates, polyandry caused females to produce significantly more offspring for a longer period of their lives. Females with greater access to males laid significantly more eggs than those mated just once, and polyandrous females had a longer oviposition period than once mated females. Polyandrous females lived significantly longer than both virgin and serially monogamous females, suggesting that costs of mating are either low or offset by other benefits. A statistically significant interaction between the number of matings and mating treatment showed that additional matings allowed fitness increases for polyandrous, but not serially monogamous, flies. A direct fitness benefit for females by sperm replenishment is the most likely explanation for these results. Males may have partitioned their sperm and/or seminal fluid protein contributions to provide less for females they previously mated (i.e., the Coolidge effect), but male ejaculate exploitation and female effects are also possible. The high benefits and low costs of polyandry in our study contrast with other Drosophila papers and therefore highlight the extreme mating system diversity across the genus.

Significance statement

In most mating systems, it is unclear why females mate with more than one male. Fruit fly females generally are expected to experience severe costs of mating. We used a highly promiscuous fruit fly species to test for costs and benefits to females of remaining virgins, mating once, remating many times with the same male (monogamy), and remating several times with a different male (polyandry). Polyandry was advantageous for females over monogamy because it allowed them to produce more adult offspring for a longer period of their lives. Additional copulations resulted in strong fitness increases for polyandrous, but not monogamous, female flies. Both polyandry and monogamy were better than mating just once because they allowed increases in egg and offspring production. Polyandry also conferred increases in lifespan over both virginity and monogamy. Therefore, we show benefits to mating with multiple males and failed to observe substantial costs of mating. The most likely explanation for our findings is a male effect by which they transfer fewer sperm and/or other ejaculate components to females they have previously mated (the Coolidge effect), though other mechanisms are possible.

Keywords

Monogamy Virginity Polyandry Sperm allocation Cost of mating Coolidge effect 

Notes

Acknowledgements

We thank N.R. Schroeder and J.A. Gómez for their help in handling flies and media preparation. S. Pitnick provided helpful comments on an earlier draft. Materials and other support were provided by the Department of Biological Sciences and Office of Research and Graduate Studies at Florida Gulf Coast University.

References

  1. Abraham S, Vera MT, Perez-Staples D (2015) Current sperm competition determines sperm allocation in a tephritid fruit fly. Ethology 121:451–461Google Scholar
  2. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164Google Scholar
  3. Bateman AJ (1948) Intrasexual selection in Drosophila. Heredity 2:349–368Google Scholar
  4. Bezzerides AL, Iyengar VK, Eisner T (2008) Female promiscuity does not lead to increased fertility or fecundity in an arctiid moth (Utetheisa ornatrix). J Insect Behav 21:213–221Google Scholar
  5. Boulton RA, Shuker DM (2016) Polyandry is context dependent but not convenient in a mostly monandrous wasp. Anim Behav 112:119–125Google Scholar
  6. Bretman A, Fricke C, Hetherington P, Stone R, Chapman T (2010) Exposure to rivals and plastic responses to sperm competition in Drosophila melanogaster. Behav Ecol 21:317–321Google Scholar
  7. Bretman A, Gage MJG, Chapman T (2011) Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol Evol 26:467–473Google Scholar
  8. Bretman A, Westmancoat JD, Gage MJG, Chapman T (2012) Costs and benefits of lifetime exposure to mating rivals in Drosophila melanogaster. Evolution 67:2413–2422Google Scholar
  9. Bretman A, Westmancoat JD, Gage MJG, Chapman T (2013) Individual plastic responses by males to rivals reveal mismatches between behavior and fitness outcomes. Proc R Soc Lond B 279:2868–2876Google Scholar
  10. Briefer EF, Farrell ME, Hayden TJ, McElligott AG (2013) Fallow deer polyandry is related to fertilization insurance. Behav Ecol Sociobiol 67:657–665Google Scholar
  11. Brown WD, Bjork A, Schneider K, Pitnick S (2004) No evidence that polyandry benefits females in Drosophila melanogaster. Evolution 58:1242–1250Google Scholar
  12. Bundgaard J, Barker JSF (2000) Remating, sperm transfer, and sperm displacement in the cactophilic species Drosophila buzzatii Patterson & Wheeler (Diptera : Drosophilidae). Biol J Linn Soc 71:145–164Google Scholar
  13. Byrne PG, Rice GR, Rice WR (2008) Effect of a refuge from persistent male courtship in the Drosophila laboratory environment. Integr Comp Biol 48:E1–E7Google Scholar
  14. Caspers BA, Krause ET, Hendrix R, Kopp M, Rupp O, Rosentreter K, Steinfartz S (2014) The more the better—polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra). Mol Ecol 23:239–250Google Scholar
  15. Castrezana S, Faircloth BC, Bridges WC, Gowaty PA (2017) Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males in Drosophila melanogaster. Ecol Evol 7:7515–7526Google Scholar
  16. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244Google Scholar
  17. Chelini MC, Hebets EA (2016) Polyandry in the absence of fitness benefits in a species with female-biased sexual size dimorphism. Anim Behav 119:213–222Google Scholar
  18. Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365Google Scholar
  19. Crawley MJ (2012) The R book, 2nd ed. Wiley, West SussexGoogle Scholar
  20. Croshaw DA, Pechmann JHK, Glenn TC (2017) Multiple paternity benefits female marbled salamanders by increasing survival of progeny to metamorphosis. Ethology 123:307–315Google Scholar
  21. De Loof A (2011) Longevity and aging in insects: is reproduction costly; cheap; beneficial or irrelevant? A critical evaluation of the “trade-off” concept. J Insect Physiol 57:1–11Google Scholar
  22. Dewsbury DA (1981) Effects of novelty on copulatory behavior: the Coolidge effect and related phenomena. Psychol Bull 89:464–482Google Scholar
  23. Droge-Young EM, Belote JM, Eeswara A, Pitnick S (2016) Extreme ecology and mating system: discriminating among direct benefits models in red flour beetles. Behav Ecol 27:575–583Google Scholar
  24. Edvardsson M (2007) Female Callosobruchus maculatus mate when they are thirsty: resource-rich ejaculates as mating effort in a beetle. Anim Behav 74:183–188Google Scholar
  25. Eizaguirre C, Laloi D, Massot M, Richard M, Federici P, Clobert J (2007) Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard. Proc R Soc Lond B 274:425–430Google Scholar
  26. Fisher DN, Doff RJ, Price TAR (2013) True polyandry and pseudopolyandry: why does a monandrous fly remate? BMC Evol Biol 13:157Google Scholar
  27. Fowler K, Partridge L (1989) A cost of mating in female fruit flies. Nature 338:760–761Google Scholar
  28. Fricke C, Bretman A, Chapman T (2010) Female nutritional status determines the magnitude and sign of responses to a male ejaculate signal in Drosophila melanogaster. J Evol Biol 23:157–165Google Scholar
  29. Goenaga J, Mensch J, Fanara JJ, Hasson E (2012) The effect of mating on starvation resistance in natural populations of Drosophila melanogaster. Evol Ecol 26:813–823Google Scholar
  30. Good JM, Ross CL, Markow TA (2006) Multiple paternity in wild-caught Drosophila mojavensis. Mol Ecol 15:2253–2260Google Scholar
  31. Gowaty PA (2013) Adaptively flexible polyandry. Anim Behav 86:877–884Google Scholar
  32. Gowaty PA, Kim YK, Rawlings J, Anderson WW (2010) Polyandry increases offspring viability and mother productivity but does not decrease mother survival in Drosophila pseudoobscura. Proc Natl Acad Sci U S A 107:13771–13776Google Scholar
  33. Gowaty PA, Kim YK, Anderson WW (2012) No evidence of sexual selection in a repetition of Bateman's classic study of Drosophila melanogaster. Proc Natl Acad Sci U S A 109:11740–11745Google Scholar
  34. Gowaty PA, Kim YK, Anderson WW (2013) Mendel’s law reveals fatal flaws in Bateman's 1948 study of mating and fitness. Fly 7:28–38Google Scholar
  35. Harano T (2012) Water availability affects female remating in the seed beetle, Callosobruchus chinensis. Ethology 118:925–931Google Scholar
  36. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64Google Scholar
  37. Johnson SL, Brockmann HJ (2013) Parental effects on early development: testing for indirect benefits of polyandry. Behav Ecol 24:1218–1228Google Scholar
  38. Kelleher ES, Markow TA (2007) Reproductive tract interactions contribute to isolation in Drosophila. Fly 1:33–37Google Scholar
  39. Kelly CD, Jennions MD (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol Rev 86:863–884Google Scholar
  40. King BH, Bressac C (2010) No fitness consequence of experimentally induced polyandry in a monandrous wasp. Behaviour 147:85–102Google Scholar
  41. Knowles LL, Markow TA (2001) Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila. Proc Natl Acad Sci U S A 98:8692–8696Google Scholar
  42. Knowles LL, Hernandez BB, Markow TA (2005) Nonantagonistic interactions between the sexes revealed by the ecological consequences of reproductive traits. J Evol Biol 18:156–161Google Scholar
  43. Kotiaho JS, Simmons LW (2003) Longevity cost of reproduction for males but no longevity cost of mating or courtship for females in the male-dimorphic dung beetle Onthophagus binodis. J Insect Physiol 49:817–822Google Scholar
  44. Kuijper B, Stewart AD, Rice WR (2006) The cost of mating rises nonlinearly with copulation frequency in a laboratory population of Drosophila melanogaster. J Evol Biol 19:1795–1802Google Scholar
  45. Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Natl Acad Sci U S A 101:6530–6535Google Scholar
  46. Lemaitre JF, Gaillard JM (2013) Polyandry has no detectable mortality cost in female mammals. PLoS One 8:e66670Google Scholar
  47. Liu XP, He HM, Kuang XJ, Xue FS (2010) A comparison of female fitness between monogamy and polyandry in the cabbage beetle, Colaphellus bowringi. Anim Behav 79:1391–1395Google Scholar
  48. Manier MK, Belote JM, Berben KS, Lupold S, Ala-Honkola O, Collins WF, Pitnick S (2013) Rapid diversification of sperm precedence traits and processes among three sibling Drosophila species. Evolution 67:2348–2362Google Scholar
  49. Markow TA (1982) Mating systems of cactophilic Drosophila. In: Barker JSF, Starmer WT (eds) Ecological genetics and evolution. The cactus-yeast-Drosophila model system. Academic Press Australia, Sydney, pp 273–287Google Scholar
  50. Markow TA (1996) Evolution of Drosophila mating systems. Evol Biol 29:73–106Google Scholar
  51. Markow TA (2011) “Cost” of virginity in wild Drosophila melanogaster females. Ecol Evol 1:596–600Google Scholar
  52. Markow TA, Ankney PF (1984) Drosophila males contribute to oogenesis in a multiple mating species. Science 224:302–303Google Scholar
  53. Markow TA, O’Grady PM (2005) Evolutionary genetics of reproductive behavior in Drosophila: connecting the dots. Annu Rev Genet 39:263–291Google Scholar
  54. Markow TA, Gallagher PD, Krebs RA (1990) Ejaculate-derived nutritional contribution and female reproductive success in Drosophila mojavensis (Patterson and Crow). Funct Ecol 4:67–73Google Scholar
  55. Markow TA, Beall S, Castrezana S (2012) The wild side of life: Drosophila reproduction in nature. Fly 6:98–101Google Scholar
  56. Osikowski A, Rafinski J (2001) Multiple insemination increases reproductive success of female Montandon’s newt (Triturus montandoni, Caudata, Salamandridae). Behav Ecol Sociobiol, 49:145–149Google Scholar
  57. Pai A, Bennett L, Yan GY (2005) Female multiple mating for fertility assurance in red flour beetles (Tribolium castaneum). Can J Zool 83:913–919Google Scholar
  58. Pai A, Feil S, Yan G (2007) Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum. Evol Ecol 21:687–702Google Scholar
  59. Perez-Staples D, Aluja M (2006) Sperm allocation and cost of mating in a tropical tephritid fruit fly. J Insect Physiol 52:839–845Google Scholar
  60. Pitnick S, Garcia-Gonzalez F (2002) Harm to females increases with male body size in Drosophila melanogaster. Proc R Soc Lond B 269:1821–1828Google Scholar
  61. Pitnick S, Markow TA, Spicer GS (1995) Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci U S A 92:10614–10618Google Scholar
  62. Pitnick S, Spicer GS, Markow T (1997) Phylogenetic examination of female incorporation of ejaculate in Drosophila. Evolution 51:833–845Google Scholar
  63. Pizzari T (2002) Sperm allocation, the Coolidge effect and female polyandry. Trends Ecol Evol 17:456–456Google Scholar
  64. Pizzari T, Cornwallis CK, Lovlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74Google Scholar
  65. Pound N, Gage MJG (2004) Prudent sperm allocation in Norway rats, Rattus norvegicus: a mammalian model of adaptive ejaculate adjustment. Anim Behav 68:819–823Google Scholar
  66. Priest NK, Galloway LF, Roach DA (2008) Mating frequency and inclusive fitness in Drosophila melanogaster. Am Nat 171:10–21Google Scholar
  67. Reguera P, Pomiankowski A, Fowler K, Chapman T (2004) Low cost of reproduction in female stalk-eyed flies, Cyrtodiopsis dalmanni. J Insect Physiol 50:103–108Google Scholar
  68. Rovelli V, Randi E, Davoli F, Macale D, Bologna MA, Vignoli L (2015) She gets many and she chooses the best: polygynandry in Salamandrina perspicillata (Amphibia: Salamandridae). Biol J Linn Soc 116:671–683Google Scholar
  69. SAS Institute (2003) SAS system for Windows. Release 8.01 edition. SAS Institute, CaryGoogle Scholar
  70. Sheldon BC (1994) Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257:25–30Google Scholar
  71. Sirot LK, Wolfner MF, Wigby S (2011) Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. Proc Natl Acad Sci U S A 108:9922–9926Google Scholar
  72. Snook RR, Hosken DJ (2004) Sperm death and dumping in Drosophila. Nature 428:939–941Google Scholar
  73. Spence R, Reichard M, Smith C (2013) Strategic sperm allocation and a Coolidge effect in an externally fertilizing species. Behav Ecol 24:82–88Google Scholar
  74. Tan CKW, Lovlie H, Greenway E, Goodwin SF, Pizzari T, Wigby S (2013) Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila. Proc R Soc Lond B 280Google Scholar
  75. Tang-Martinez Z (2016) Rethinking Bateman's principles: challenging persistent myths of sexually reluctant females and promiscuous males. J Sex Res 53:532–559Google Scholar
  76. Taylor ML, Wigmore C, Hodgson DJ, Wedell N, Hosken DJ (2008) Multiple mating increases female fitness in Drosophila simulans. Anim Behav 76:963–970Google Scholar
  77. Taylor ML, Price TAR, Wedell N (2014) Polyandry in nature: a global analysis. Trends Ecol Evol 29:376–383Google Scholar
  78. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar
  79. Valimaki P, Kaitala A, Kokko H (2006) Temporal patterns in reproduction may explain variation in mating frequencies in the green-veined white butterfly Pieris napi. Behav Ecol Sociobiol 61:99–107Google Scholar
  80. Wang Q, Davis LK (2006) Females remate for sperm replenishment in a seed bug: Evidence from offspring viability. J Insect Behav 19:337–346Google Scholar
  81. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320Google Scholar
  82. Whittingham LA, Dunn PO (2010) Fitness benefits of polyandry for experienced females. Mol Ecol 19:2328–2335Google Scholar
  83. 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 19:751–757Google Scholar
  84. Worthington AM, Kelly CD (2016) Direct costs and benefits of multiple mating: are high female mating rates due to ejaculate replenishment? Behav Process 124:115–122Google Scholar
  85. Wright LI, Fuller WJ, Godley BJ, McGowan A, Tregenza T, Broderick AC (2013) No benefits of polyandry to female green turtles. Behav Ecol 24:1022–1029Google Scholar
  86. Zhao M, Li CL, Zhang W, Wang H, Luo ZH, Gu Q, Gu ZR, Liao CL, Wu H (2016) Male pursuit of higher reproductive success drives female polyandry in the Omei treefrog. Anim Behav 111:101–110Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesFlorida Gulf Coast UniversityFort MyersUSA

Personalised recommendations