Evolutionary Ecology

, Volume 24, Issue 1, pp 39–47 | Cite as

Differential susceptibility to food stress in neonates of sexual and asexual mollies (Poecilia, Poeciliidae)

  • Michael Tobler
  • Ingo Schlupp
Original Paper


The maintenance of sex is still an evolutionary puzzle given its immediate costs. Stably coexisting complexes of asexually and sexually reproducing forms allow to study mechanisms that balance the costs and benefits of both asexual and sexual reproduction. Here, we tested whether coexisting asexual and sexual fish of the genus Poecilia differed in neonate mortality when exposed to environmental stress in the form of fluctuating temperatures and food deprivation. We find that asexual Amazon mollies, Poecilia formosa, are significantly more sensitive to food stress than their sexual relative Poecilia latipinna, but both are equally unaffected by variable temperatures. Differences in the susceptibility to environmental stress may contribute to diminishing the asexuals’ benefits of a higher intrinsic population growth rate and thus mediate stable coexistence of the two reproductive forms.


Asexuality Evolution and maintenance of sex Gynogenesis Environmental stress Mutation accumulation 



We thank Tami Thomason and Wendal Porter for technical support. This research project was approved by the Animal Care and Use Committee of the University of Oklahoma (AUS R05-014). Texas Parks & Wildlife issued the permit to collect fish (SPR-0305-045). Financial support came from the Basler Foundation for Biological Research, the Janggen-Poehn-Foundation, the Roche Research Foundation, and the Wolfermann-Nägeli-Foundation (to M.T.) as well as the University of Oklahoma Faculty Senate (to I.S.).


  1. Balsano JS, Rasch EM, Monaco PJ (1989) The evolutionary ecology of Poecilia formosa and its triploid associate. In: Meffe GK, Snelson FF (eds) Ecology and evolution of lifebearing fishes (Poeciliidae). Prentice Hall, New Jersey, pp 277–297Google Scholar
  2. Barton NH, Charlesworth B (1998) Why sex and recombination? Science 281:1986–1990. doi: 10.1126/science.281.5385.1986 CrossRefPubMedGoogle Scholar
  3. Bell G (1982) The masterpiece of nature, the evolution and genetics of sexuality. University of California Press, BerkeleyGoogle Scholar
  4. Buckling A, Wei Y, Massey RC, Brockhurst MA, Hochberg ME (2006) Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proc R Soc B Biol Sci 273:45–49. doi: 10.1098/rspb.2005.3279 CrossRefGoogle Scholar
  5. Charlesworth B (1990) Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet Res 55:199–221CrossRefPubMedGoogle Scholar
  6. Choleva L, Apostolou A, Rab P, Janko K (2008) Making it on their own: sperm-dependent hybrid fishes (Cobitis) switch the sexual host and expand beyond the ranges of their original sperm donors. Philos Trans R Soc Lond B Biol Sci 363:2911–2919. doi: 10.1098/rstb.2008.0059 CrossRefPubMedGoogle Scholar
  7. Constantz GD (1989) Reproductive biology of poeciliid fishes. In: Meffe GK, Snelson FF (eds) Ecology and evolution of livebearing fishes (Poeciliidae). Prentice Hall, New Jersey, pp 33–50Google Scholar
  8. Cooper T, Lenski R, Elena S (2005) Parasites and mutational load: an experimental test of the pluralistic theory for the evolution of sex. Proc R Soc B Biol Sci 272:311–317CrossRefGoogle Scholar
  9. Dawley RM (1989) An introduction to unisexual vertebrates. In: Dawley RM, Bogart JP (eds) Evolution and ecology of unisexual vertebrates. Bulletin 466. New York State Museum, New York, pp 1–18Google Scholar
  10. Gabriel W, Bürger R (2000) Fixation of clonal lineages under Muller’s ratchet. Evol Int J Org Evol 54:1116–1125Google Scholar
  11. Gabriel W, Lynch M, Bürger R (1993) Muller’s ratchet and mutational meltdowns. Evol Int J Org Evol 47:1744–1757. doi: 10.2307/2410218 Google Scholar
  12. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290. doi: 10.2307/3544435 CrossRefGoogle Scholar
  13. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci USA 87:3566–3573. doi: 10.1073/pnas.87.9.3566 CrossRefPubMedGoogle Scholar
  14. Heubel K (2004) Population ecology and sexual preferences in the mating complex of the unisexual Amazon molly Poecilia formosa (Girard, 1859). Dissertation, Universität HamburgGoogle Scholar
  15. Hubbs C (1964) Interactions between a bisexual fish species and its gynogenetic sexual parasite. Bull Tex Mem Mus 8:1–72Google Scholar
  16. Killick S, Carlsson A, West S, Little T (2006) Testing the pluralist approach to sex: the influence of environment on synergistic interactions between mutation load and parasitism in Daphnia magna. J Evol Biol 19:1603–1611. doi: 10.1111/j.1420-9101.2006.01123.x CrossRefPubMedGoogle Scholar
  17. Kokko H, Heubel KU, Rankin DJ (2008) How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites. Proc R Soc B Biol Sci 275:817–825CrossRefGoogle Scholar
  18. Kondrashov AS (1982) Selection against harmful mutations in large asexual and sexual populations. Genet Res 40:325–332CrossRefPubMedGoogle Scholar
  19. Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336:435–441. doi: 10.1038/336435a0 CrossRefPubMedGoogle Scholar
  20. Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:372–387PubMedGoogle Scholar
  21. Kondrashov AS (1999) Being too nice may be not too wise. J Evol Biol 12:1031. doi: 10.1046/j.1420-9101.1999.00127.x CrossRefGoogle Scholar
  22. Kondrashov AS, Houle D (1994) Genotype-environment interactions and the estimation of the genomic mutation rate in Drosophila melanogaster. Proc R Soc B Biol Sci 258:221–227CrossRefGoogle Scholar
  23. Ladle RJ (1992) Parasites and sex: catching the Red Queen. Trends Ecol Evol 7:405–408. doi: 10.1016/0169-5347(92)90021-3 CrossRefGoogle Scholar
  24. Lampert KP, Schartl M (2008) The origin and evolution of a unisexual hybrid: Poecilia formosa. Philos Trans R Soc Lond B Biol Sci 363:2901–2909. doi: 10.1098/rstb.2008.0040 CrossRefPubMedGoogle Scholar
  25. Lampert KP, Lamatsch DK, Epplen JT, Schartl M (2005) Evidence for a monophyletic origin of triploid clones of the Amazon molly, Poecilia formosa. Evol Int J Org Evol 59:881–889Google Scholar
  26. Lively CM (1989) Adaptation by a parasitic trematode to local populations of its snail host. Evol Int J Org Evol 43:1663–1671. doi: 10.2307/2409382 Google Scholar
  27. Lively CM, Lloyd DG (1990) The cost of biparental sex under individual selection. Am Nat 135:489–500. doi: 10.1086/285058 CrossRefGoogle Scholar
  28. Lively CM, Craddock C, Vrijenhoek RC (1990) Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864–867. doi: 10.1038/344864a0 CrossRefGoogle Scholar
  29. Lively C, Lyons E, Peters A, Jokela J (1998) Environmental stress and the maintenance of sex in a freshwater snail. Evol Int J Org Evol 52:1482–1486. doi: 10.2307/2411317 Google Scholar
  30. Loewe L, Lamatsch DK (2008) Quantifying the threat of extinction from Muller’s ratchet in the diploid Amazon molly (Poecilia formosa). BMC Evol Biol 8:88. doi: 10.1186/1471-2148-8-88 CrossRefPubMedGoogle Scholar
  31. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, CambridgeGoogle Scholar
  32. Niemeitz A, Kreutzfeldt R, Schartl M, Schlupp I (2002) Male mating behaviour of a molly, Poecilia latipunctata: a third host for the sperm-dependent Amazon molly, Poecilia formosa. Acta Ethol 5:45–49. doi: 10.1007/s10211-002-0065-2 CrossRefGoogle Scholar
  33. Riesch R, Schlupp I, Plath M (2008) Female sperm limitation in natural populations of a sexual/asexual mating complex (Poecilia latipinna, Poecilia formosa). Biol Lett 4:266–269. doi: 10.1098/rsbl.2008.0019 CrossRefPubMedGoogle Scholar
  34. Ryan MJ, Dries LA, Batra P, Hillis DM (1996) Male mate preferences in a gynogenetic species complex of Amazon mollies. Anim Behav 52:1225–1236. doi: 10.1006/anbe.1996.0270 CrossRefGoogle Scholar
  35. Salathé M, Kouyos RD, Bonhoeffer S (2008) The state of affairs in the kingdom of the Red Queen. Trends Ecol Evol 23:439–445. doi: 10.1016/j.tree.2008.04.010 CrossRefPubMedGoogle Scholar
  36. Schartl M, Wilde B, Schlupp I, Parzefall J (1995) Evolutionary origin of a parthenoform, the Amazon molly Poecilia formosa, on the basis of a molecular genealogy. Evol Int J Org Evol 49:827–835. doi: 10.2307/2410406 Google Scholar
  37. Schlupp I (2005) The evolutionary ecology of gynogenesis. Annu Rev Ecol Evol Syst 36:399–417. doi: 10.1146/annurev.ecolsys.36.102003.152629 CrossRefGoogle Scholar
  38. Schlupp I, Ryan MJ (1996) Mixed-species shoals and the maintenance of a sexual-asexual mating system in mollies. Anim Behav 52:885–890. doi: 10.1006/anbe.1996.0236 CrossRefGoogle Scholar
  39. Schories S, Lampert KP, Lamatsch DK, Garcia de Leon FJ, Schartl M (2007) Analysis of a possible independent origin of triploid P. formosa outside of the Rio Purification river system. Front Zool 4:13. doi: 10.1186/1742-9994-4-13
  40. Semlitsch RD, Hotz H, Guex G-D (1997) Competition among tadpoles of coexisting hemiclones of hybridogenetic Rana esculenta: support for the Frozen Niche Variation model. Evol Int J Org Evol 51:1249–1261. doi: 10.2307/2411054 Google Scholar
  41. Tobler M, Schlupp I (2005) Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the Red Queen? Biol Lett 1:166–168. doi: 10.1098/rsbl.2005.0305 CrossRefPubMedGoogle Scholar
  42. Tobler M, Schlupp I (2008) Expanding the horizon: the Red Queen and potential alternatives. Can J Zool 86:765–773. doi: 10.1139/Z08-056 CrossRefGoogle Scholar
  43. Tobler M, Wahli T, Schlupp I (2005) Comparison of parasite communities in native and introduced populations of sexual and asexual mollies of the genus Poecilia. J Fish Biol 67:1072–1082. doi: 10.1111/j.0022-1112.2005.00810.x CrossRefGoogle Scholar
  44. Vrijenhoek RC (1979) Factors affecting clonal diversity and coexistence. Am Zool 19:787–789Google Scholar
  45. Vrijenhoek RC (1994) Unisexual fish: model systems for studying ecology and evolution. Annu Rev Ecol Syst 25:71–96. doi: 10.1146/ CrossRefGoogle Scholar
  46. Vrijenhoek RC, Pfeiler E (1997) Differential survival of sexual and asexual Poeciliopsis during environmental stress. Evol Int J Org Evol 51:1593–1600. doi: 10.2307/2411211 Google Scholar
  47. West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12:1003–1012. doi: 10.1046/j.1420-9101.1999.00119.x CrossRefGoogle Scholar
  48. Wetherington JD, Schenck RA, Vrijenhoek RC (1989) The origins and ecological success of unisexual Poeciliopsis: the frozen niche-variation modell. In: Meffe GK, Snelson FF (eds) Ecology and evolution of lifebearing fishes (Poeciliidae). Prentice Hall, New Jersey, pp 259–275Google Scholar
  49. Wolfe L (1993) Inbreeding depression in Hydrophyllum appendiculatum: role of maternal effects, crowding, and parental mating history. Evol Int J Org Evol 47:374–386. doi: 10.2307/2410058 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Institute of ZoologyUniversity of ZürichZürichSwitzerland
  2. 2.Department of ZoologyUniversity of OklahomaNormanUSA
  3. 3.Department of Biology and Department of Wildlife and Fisheries SciencesTexas A&M UniversityCollege StationUSA

Personalised recommendations