Behavioral Ecology and Sociobiology

, Volume 60, Issue 2, pp 159–165 | Cite as

Black spots and female association preferences in a sexual/asexual mating complex (Poecilia, Poeciliidae, Teleostei)

  • Michael Tobler
  • Martin Plath
  • Heike Burmeister
  • Ingo Schlupp
Original Article


We investigated whether female association preferences for males are influenced by black spot disease (BSD), a parasite induced change of the host phenotype. We compared three different species of fish: a gynogenetic hybrid species, Poecilia formosa (amazon molly) and two sexual species (Poecilia latipinna and Poecilia mexicana), which were involved in the natural hybridisation leading to the amazon molly. Contrary to their sexual relatives, asexual amazon mollies significantly avoided images of males infected with black spot disease. We propose that amazon molly females have direct fitness benefits from choosing healthy males. The adaptive significance of the preference for BSD-uninfected males in the asexual amazon molly is yet unclear but may involve avoidance of predation or parasite infection as well as increased sperm availability.


Black spot disease Parasites Red Queen hypothesis Sexual selection Uvulifer Video playback 



We thank Dustin Penn and Michael J. Ryan for critically reading an earlier draft of this paper. A. Taebel-Hellwig helped with the data collection; the Animal care teams of the Biozentrum Grindel; and University of Texas Brackenridge Field laboratory helped with fish care. Financial support came from DFG (SCHL 344/13-1, I. S.), from the University of Hamburg (M. P.) and from the Swiss Academy of Sciences and the NWG St. Gallen (M. T.). The experiments reported in this paper comply with the current laws in Germany. The Mexican Government kindly issued permits to collect fish (Permiso de pesca de fomento numbers: 242-219, 276/36, 210696-213-03).


  1. Able DJ (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proc Natl Acad Sci USA 93:2229–2233PubMedCrossRefGoogle Scholar
  2. Avise JC, Trexler JC, Travis J, Nelson WS (1991) Poecilia mexicana is the recent female parent of the unisexual fish P. formosa. Evolution 45:1530–1533CrossRefGoogle Scholar
  3. 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
  4. Barber I (2002) Parasites, male–male competition and female mate choice in the sand goby. J Fish Biol 61:185–198Google Scholar
  5. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B 268:71–76CrossRefGoogle Scholar
  6. Brooks B (1996) Melanin as a visual amplifier in male guppies. Naturwissenschaften 83:39–41CrossRefGoogle Scholar
  7. Brown WH (1953) Introduced fish species of the Guadalupe River Basin. Tex J Sci 2:5–25Google Scholar
  8. Bush AO, Fernández JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge Univ. Press, Cambridge, U.K.Google Scholar
  9. Endler JA, Lyles AM (1989) Bright ideas about parasites. Trends Ecol Evol 4:246–248CrossRefGoogle Scholar
  10. Gonçalves DM, Oliveira RF, Körner K, Poschadel JR, Schlupp I (2000) Using video playbacks to study visual communication in a marine fish, Salaria pavo. Anim Behav 60:351–357PubMedCrossRefGoogle Scholar
  11. Hakoyama H, Nishimura T, Matsubara N, Iguchi K (2001) Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biol J Linn Soc 72:401–407CrossRefGoogle Scholar
  12. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290CrossRefGoogle Scholar
  13. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role of parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  14. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaption to resist parasites (a review). Proc Natl Acad Sci USA 87:3566–3573PubMedCrossRefGoogle Scholar
  15. Houde AE, Torio AJ (1992) Effect of parasitic infection on male color pattern and female choice in guppies. Behav Ecol 3:346–351CrossRefGoogle Scholar
  16. Hubbs C (1964) Interactions between a bisexual fish species and its gynogenetic sexual parasite. Bull Tex Mem Mus 8:1–72Google Scholar
  17. Kennedy CE, Endler JA, Poynton SL, McMinn H (1987) Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 21:291–295CrossRefGoogle Scholar
  18. Körner KE, Lütjens O, Parzefall J, Schlupp I (1999) The role of experience in mate preferences of the unisexual amazon molly. Behaviour 136:257–268CrossRefGoogle Scholar
  19. Krause J, Godin J-GJ (1994) Influence of parasitism on the shoaling behaviour of banded killifish, Fundulus diaphanus. Can J Zool 72:1775–1779CrossRefGoogle Scholar
  20. Krause J, Godin J-GJ (1996) Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontiformes). Ethology 102:40–49Google Scholar
  21. Ladle RJ (1992) Parasites and sex: catching the Red Queen. Trends Ecol Evol 7:405–408CrossRefGoogle Scholar
  22. Landmann K, Parzefall J, Schlupp I (1999) A sexual preference in the Amazon molly, Poecilia formosa. Environ Biol Fishes 56:325–331CrossRefGoogle Scholar
  23. Lane RL, Morris JE (2000) Biology, prevention, and effects of common grubs (digenetic trematodes) in freshwater fish. Tech Bull Series 115, Iowa State UniversityGoogle Scholar
  24. Lemly AD, Esch GW (1984) Effects of the trematode Uvulifer ambloplitis on juvenile blue gill sunfish, Lepomis macrochirus: ecological implications. J Parasitol 70:475–492CrossRefGoogle Scholar
  25. Liljedal S, Folstad I, Skarstein F (1999) Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proc R Soc Lond B 266:1893–1898CrossRefGoogle Scholar
  26. Lindström K, Lundström J (2000) Male greenfinches (Carduelis chloris) with brighter ornaments have higher virus infection clearance rate. Behav Ecol Sociobiol 48:44–51CrossRefGoogle Scholar
  27. Lively CM (1987) Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 405:519–521CrossRefGoogle Scholar
  28. Lively CM, Craddock C, Vrijenhoek RC (1990) Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864–867CrossRefGoogle Scholar
  29. Marler CA, Ryan MJ (1997) Origin and maintenance of a female mating preference. Evolution 51:1244–1248CrossRefGoogle Scholar
  30. McGregor PK (2000) Playback experiments: design and analysis. Acta Ethol 3:3–8CrossRefGoogle Scholar
  31. McKinnon J (1995) Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration. Anim Behav 50:1645–1655CrossRefGoogle Scholar
  32. Meyer MK, Wischnath L, Foerster W (1985) Lebendgebärende Zierfische. Mergus Verlag, MelleGoogle Scholar
  33. Morris MR, Nicoletto P, Hesselman E (2003) A polymorphism in female preference for a polymorphic male trait in the swordtail fish Xiphophorus cortezi. Anim Behav 65:45–52CrossRefGoogle Scholar
  34. Morris MR, Rios-Cardenas O, Tudor MS (2005) Larger swordtail females prefer asymmetrical males. Biol Lett (in press)Google Scholar
  35. Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333CrossRefGoogle Scholar
  36. Nicoletto PF, Kodric-Brown A (1999) The use of digitally-modified videos to study the function of ornamentation and courtship in the guppy, Poecilia reticulata. Environ Biol Fishes 56:333–341CrossRefGoogle Scholar
  37. Oliveira RF, Rosenthal GG, Schlupp I, McGregor PK, Cuthill IC, Endler JA, Fleishman LJ, Zeil J, Barata E, Burford F, Gonçalves DM, Haley M, Jakobsson S, Jennions MD, Körner K, Lindström L, Peake T, Pilastro A, Pope DS, Roberts SGB, Rowe C, Smith J, Waas JR (2000) Considerations on the use of video playback techniques as visual stimuli: the Lisabon workshop consensus. Acta Ethol 3:61–65CrossRefGoogle Scholar
  38. Parzefall J (1969) Zur vergleichenden Ethologie verschiedener Mollienesia—Arten einschließlich einer Höhlenform von Mollienesia sphenops. Behaviour 33:1–37PubMedCrossRefGoogle Scholar
  39. Plath M (2004) Cave molly females (Poecilia mexicana) avoid parasitised males. Acta Ethol 6:47–51CrossRefGoogle Scholar
  40. Plath M, Körner KE, Parzefall J, Schlupp I (2003) Persistence of a visually mediated mating preference in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei). Subterran Biol 1:93–97Google Scholar
  41. Read AF (1988) Sexual selection and the role of parasites. Trends Ecol Evol 3:97–102CrossRefGoogle Scholar
  42. Rosenqvist G, Johansson K (1995) Male avoidance of parasitized females explained by direct benefits in a pipefish. Anim Behav 49:1039–1045CrossRefGoogle Scholar
  43. Rosenthal GG (1999) Using video playback to study sexual communication. Environ Biol Fishes 56:307–316CrossRefGoogle Scholar
  44. Rosenthal GG, Evans CS (1998) Female preferences for swords in Xiphophorus helleri reflects a bias for large apparent size. Proc Natl Acad Sci USA 95:4431–4436PubMedCrossRefGoogle Scholar
  45. Rosenthal GG, Evans CS, Miller WL (1996) Female preferences for dynamic traits in the green swordtail, Xiphophorus helleri. Anim Behav 51:811–820CrossRefGoogle Scholar
  46. Rowland WJ, Kimberly JB, Jenkins JJ, Fowler J (1995) Video playback experiments on stickleback mate choice: female motivation and attentiveness to male color cues. Anim Behav 49:1559–1567CrossRefGoogle Scholar
  47. Ryan MJ, Dries LA, Batra P, Hillis DM (1996) Male mate preferences in a gynogenetic species complex of Amazon mollies. Anim Behav 52:1225–1236CrossRefGoogle Scholar
  48. Schartl M (1995) Platyfish and swordtails: a genetic system for the analysis of molecular mechanisms in tumor formation. Trends Genet 11:185–189PubMedCrossRefGoogle Scholar
  49. 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. Evolution 49:827–835CrossRefGoogle Scholar
  50. Schlupp I (2005) The evolutionary ecology of gynogenesis. Annu Rev Ecol Evol Syst 36:399–417CrossRefGoogle Scholar
  51. Schlupp I, Nanda I, Döbler M, Lamatsch DK, Epplen JT, Parzefall J, Schmid M, Schartl A (1998) Dispensable and indispensable genes in an ameiotic fish, the Amazon molly Poecilia formosa. Cytogenet Cell Genet 80:193–198PubMedCrossRefGoogle Scholar
  52. Schlupp I, Parzefall J, Schartl M (1991) Male mate choice in mixed bisexual/unisexual breeding complexes of Poecilia (Teleostei: Poeciliidae). Ethology 88:215–222CrossRefGoogle Scholar
  53. Schlupp I, Parzefall J, Schartl M (2002) Biogeography of the Amazon molly, Poecilia formosa. J Biogeogr 29:1–6CrossRefGoogle Scholar
  54. Schlupp I, Plath M (2005) Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei). Biol Lett 1:166–168PubMedCrossRefGoogle Scholar
  55. Schlupp I, Waschulewski M, Ryan MJ (1999) Female preferences for naturally-occurring novel male traits. Behaviour 136:519–527CrossRefGoogle Scholar
  56. Seger J, Hamilton WD (1988) Parasites and sex. In: Michod RE, Levin BR (eds) The evolution of sex. Sinauer Associates, Sunderland, pp 176–193Google Scholar
  57. Simanek DE (1978) Genetic variability and population structure of Poecilia latipinna. Nature 276:612–614CrossRefGoogle Scholar
  58. Spellman SJ, Johnson AD (1987) In vitro encystment of the black spot trematode Uvulifer ambloplitis (Trematoda, Diplostomatidae). Int J Parasitol 17:897–902PubMedCrossRefGoogle Scholar
  59. Taskinen J, Kortet R (2002) Dead and alive parasites: sexual ornaments signal resistance in the male fish, Rutilus rutilus. Evol Ecol Res 4:919–929Google Scholar
  60. Taylor MI, Turner GF, Robinson RL, Stauffer JR (1998) Sexual selection, parasites and bower height skew in a bower-building cichlid fish. Anim Behav 56:379–384PubMedCrossRefGoogle Scholar
  61. Tobler M, Schlupp I (2005) Parasites in sexual and asexual molly species of the genus Poecilia (Poeciliidae, Teleostei): a case for the Red Queen? Biol Lett 1:166–168PubMedCrossRefGoogle Scholar
  62. 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 (Poecliidae, Teleostei). J Fish Biol 67:1072–1082CrossRefGoogle Scholar
  63. Turner BJ (1982) The evolutionary genetics of a unisexual fish, Poecilia formosa. In: Barigozzi C (ed) Mechanisms of speciation. Alan R. Liss, New York, pp 265–305Google Scholar
  64. Turner BJ, Balsano JS, Monaco PJ, Rasch EM (1983) Clonal diversity and evolutionary dynamics in a diploid–triploid breeding complex of unisexual fishes (Poecilia). Evolution 37:798–809CrossRefGoogle Scholar
  65. Witte K, Klink KB (2005) No preexisting bias in Sailfin molly females, Poecilia latipinna, for a sword in males. Behaviour 142:283–303CrossRefGoogle Scholar
  66. Witte K, Ueding K (2003) Sailfin molly females (Poecilia latipinna) copy the rejection of a male. Behav Ecol 14:389–395CrossRefGoogle Scholar
  67. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Michael Tobler
    • 1
  • Martin Plath
    • 2
  • Heike Burmeister
    • 3
  • Ingo Schlupp
    • 1
    • 4
  1. 1.Zoologisches InstitutUniversität ZürichZürichSwitzerland
  2. 2.Institut für Biochemie/BiologieUniversität PotsdamPotsdamGermany
  3. 3.Biozentrum GrindelUniversität HamburgHamburgGermany
  4. 4.Department of ZoologyUniversity of OklahomaNormanUSA

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