Environmental Biology of Fishes

, Volume 47, Issue 4, pp 345–352 | Cite as

Polygynandry inPseudotropheus zebra, a cichlid fish from Lake Malawi

  • Alex Parker
  • Irv Kornfield
Full paper


Parental care in the Malawian cichlid fishPseudotropheus zebra ‘BB’ is extensive and exclusively maternal; males contribute only genetic material. The costs of searching for multiple mates (in this case risk of predation on orally incubated eggs) suggested that females should be monandrous; microsatellite genetypes of seven brooding females and their young, however, reveal extensive multiple paternity in this species, with a mean of 3.8 paternal individuals per brood. Polygynandry inP. zebra is probably not maintained by selection for genetically diverse offspring; potential explanations include avoidance of inbreeding, and bet-hedging on other male characteristics that females are unable to evaluate when selecting a mate. The observed degree of multiple paternity strongly suggests that females are free to choose mates as they will, a prerequisite of many theories positing sexual selection as a key element in Malawi chichlid evolution. It should also result in elevation of effective population sizes, and thus be antagonistic to runaway evolution of male secondary sexual characteristics, but not necessarily to other modes of sexual selection.

Key words

Microsatellites Paternity Bet-hedging Sexual selection 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Alcock, J. 1989. Animal behavior. Sinauer Associates, Sunderland. 596 pp.Google Scholar
  2. Arnold, S.J. 1983. Sexual selection: the interface of theory and empiricism. pp. 67–108. In: P. Bateson (ed.) Mate Choice. Cambridge University Press, Cambridge.Google Scholar
  3. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith & K. Struhl (ed.). 1989. Short protocols in molecular biology. John Wiley & Sons. New York. 387 pp.Google Scholar
  4. Avise, J. 1994. Molecular markers, natural history, and evolution, Sinauer Associates, Sunderland. 511 pp.Google Scholar
  5. Barlow, G.W. 1991. Mating systems among cichlid fishes. pp. 173–190. In: M.H.A. Keenleyside (ed.) Cichlid Fishes. Chapman & Hall, London.Google Scholar
  6. Chakraborty, R., T.R. Meagher & P.E. Smouse. 1988. Parentage analysis with genetic markers in natural populations. I. The expected proportion of offspring with unambiguous paternity. Genetics 118: 527–536.Google Scholar
  7. Devlin, B., K. Roeder & N.C. Ellstrand. 1990. Fractional paternity assignment: theoretical development and comparison to other methods. Theor. Appl. Genet. 76: 369–380.Google Scholar
  8. Dixon, A.F.G. 1989. Evolution and adaptive significance of cyclical parthenogenesis in aphids. pp. 289–297. In: A.J. Minks & P. Harrewijn (ed.) Aphids, Their Biology, Natural Enemies, and Control, Elsevier, Amsterdam.Google Scholar
  9. Dominey, W.J. 1984. Effects of sexual selection and life history on speciation: species flocks in African cichlids and HawaiianDrosophila. pp. 231–250. In: A.A. Echelle & I. Kornfield (ed.) Evolution of Fish Species Flocks. University of Maine Press, Orono.Google Scholar
  10. Eccles, D.H. & E. Trewavas. 1989. Malawian cichlid fishes. Lake Fish Movies, Herten. 334 pp.Google Scholar
  11. Ellstrand, N.C. 1984. Multiple paternity in the fruits of the wild radishRaphanus sativus. Amer. Nat. 123: 819–828.Google Scholar
  12. Fryer, G. & T.D. Iles. 1972. The cichlid fishes of the Great Lakes of Africa. Oliver Boyd, Edinborough. 641 pp.Google Scholar
  13. Glesener, R.R. & D. Tilman. 1978. Sexuality and the components of environmental uncertainty. Amer. Nat. 112: 659–673.Google Scholar
  14. Hardy, I.C.W. 1994. Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos 69: 3–20.Google Scholar
  15. Hert, E. 1992. Homing and home-site fidelity in rock-dwelling cichlids. Env. Biol. Fish. 33: 229–237.Google Scholar
  16. Kirkpatrick, M. & M.J. Ryan. 1991. The evolution of mating preferences and the paradox of the lek. Nature 350: 33–38.Google Scholar
  17. Konings, A. 1990. Cichlids of Lake Malawi. TFH Publications. Neptune City. 495 pp.Google Scholar
  18. Korings, A. 1995. Malawi cichlids in their natural habitat, Cichlid Press, St. Leon-Rot. 352 pp.Google Scholar
  19. Kornfield, I. 1991. Genetics, pp. 103–128. In: M.H.A. Keenleyside (ed.) Cichlid Fishes, Chapman & Hall, London.Google Scholar
  20. Kornfield, I. & A. Parker, 1996. Molecular systematics of a rapidly evolving species flock: the mbuna of Lake Malawi and the search for phylogenetic signal. In: T.D. Kocher & C. Stepien (ed.) Molecular Systematics of Fishes, Academic Press, New York (in press).Google Scholar
  21. Lewis, D.S.C., P.N. Reinthal & J. Trendall. 1986. A guide to the fishes of Lake Malawi National Park. World Wildlife Foundation. Gland. 71 pp.Google Scholar
  22. Lincoln, S. & M. Daly. 1991. PCPRIMER (computer software). Whitehead Institute, Cambridge.Google Scholar
  23. Marsh & A.J. Ribbink. 1986. Reproductive seasonality in a group of rock-frequenting cichlids in Lake Malawi. J. Zool. Soc. Lond. 209: 9–20.Google Scholar
  24. McElroy, D.M. & I. Kornfield. 1990. Sexual selection, reproductive behavior, and speciation in the mbuna species flock of lake Malawi. Env. Biol. Fish. 28: 273–284.Google Scholar
  25. McKaye, K.R. 1991. Sexual selection and the evolution of the cichlid fishes of Lake Malawi. pp. 241–257. In: M.H.A. Keenleyside (ed.) Cichlid Fishes, Chapman & Hall, London.Google Scholar
  26. McKaye, K.R. & W.N. Gray, 1984. Extrinsic barriers to gene flow in rock dwelling cichlids of Lake Malawi: microhabitat heterogenecity and reef colonization. pp. 169–184. In: A.A. Echelle & I. Kornfield (ed.) Evolution of Fish Species Flocks, University of Maine Press, Orono.Google Scholar
  27. Meyer, A., T.D. Kocher, P. Basasibwaki & A.C. Wilson. 1990. Monophyletic origin of Lake Victoria cichlids suggested by mitochondrial DNA sequences. Nature 347: 550–553.Google Scholar
  28. Milligan, B.G. & C.K. McMurray. 1993. Dominant vs. codominant genetic markers in the estimation ot male mating success. Mol. Ecol. 2: 275–283.Google Scholar
  29. Moran, P. & I. Kornfield. 1993. Retention of an ancestral polymorphism in the mbuna species flock (Pisces: Cichlidae) of Lake Malawi. Mol. Biol. Evol. 10: 1015–1029.Google Scholar
  30. Moran, P. & I. Kornfield. 1995. Evidence of a population bottleneck and extreme philopatry in the mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol. Biol. Evol. 12: 1085–1093.Google Scholar
  31. Moran, P., I. Kornfield & P. Reinthal. 1994. Molecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake Malawi. Copeia 1994: 274–228.Google Scholar
  32. Mrowka, W. 1987. Oral fertilization in a mouthbrooding cichlid fish. Ethology 74: 293–296.Google Scholar
  33. Nichols, R.A. & R.K. Butlin. 1989. Does runaway sexual selection work in finite populations? J. Evol. Biol. 2: 299–313.Google Scholar
  34. Noakes, D.L.G. 1991. Ontogeny of behavior in cichlids. pp. 209–224. In: M.H.A. Keenleyside (ed.) Cichlid Fishes, Chapman & Hall, London.Google Scholar
  35. Owen, R.B., R. Crossley, T.C. Johnson, D. Tweddle, I. Kornfield, S. Davison, D.H. Eccles & D.E. Engstrom. 1990. Major low levels of Lake Malawi and implications for speciation rates in cichlid fishes. Proc. Roy. Soc. Lond. 240-B: 519–553.Google Scholar
  36. Parker, G.A. 1983. Mate quality and mating decisions. pp. 141–166. In: P. Bateson (ed.) Mate Choice, Cambridge University Press, Cambridge.Google Scholar
  37. Parker, G.A. 1984. Sperm competition and the evolution of animal mating strategies, pp. 1–60. In: R.L. Smith (ed.) Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, Orlando.Google Scholar
  38. Parker, G.A. 1992. Snakes and female sexuality. Nature 355: 395–396.Google Scholar
  39. Philippi, T. & J. Seger. 1989. Hedging one's evolutionary bets, revisited. Trends Ecol. Evol. 4: 41–44.Google Scholar
  40. Queller, D.C., J.E. Strassmann & C.R. Hughes. 1993. Microsatellites and kinship. Trends Ecol. Evol. 8; 285–288.Google Scholar
  41. Ribbink, A.J. & D.S.C. Lewis. 1982.Melanochromis crabro sp. nov.: a cichlid fish from Lake Malawi which feeds on ectoparasites and catfish eggs. Neth. J. Zool. 32: 72–87.Google Scholar
  42. Ribbink, A.J., B.A. Marsh, A.C. Marsh, A.C. Ribbink & B.J. Sharp. 1983. A preliminary survey of the cichlid fishes of rocky habitats of Lake Malawi. S. Afr. J. Sci. 18: 149–310.Google Scholar
  43. Row, L., G. Arnquist & J.J. Kruppa. 1994. Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol. Evol. 9: 289–294.Google Scholar
  44. Scholz, C.A. & B.R. Rosendahl. 1988. Low lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data. Science 240: 1645–1648.Google Scholar
  45. Sugg, D.W. & R.K. Chesser. 1994. Effective population sizes with multiple paternity. Genetics 137: 1147–1155.Google Scholar
  46. Taborsky, M. 1994. Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv. Stud. Behav. 23: 1–100.Google Scholar
  47. Trendall, K. 1988. Recruitment of juvenile mbuna (Pisces: Cichlidae) to experimental rock shelters in Lake Malawi, Africa, Env. Biol. Fish. 22: 117–131.Google Scholar
  48. Trivers, R.L. 1985. Social evolution. Benjamin/Cummings Publishing, Menlo Park. 462 pp.Google Scholar
  49. Turner, G.F. 1994. Speciation mechanisms in Lake Malawi cichlids: a critical review. Arch. Hydrobiol. 44: 139–160.Google Scholar
  50. Watson, P.J. 1991. Multiple paternity as genetic bet-hedging in female Sierra Dome spiders,Lynyphia litigiosa. Anim. Behav. 41: 343–360.Google Scholar
  51. Wilcockson, R.W., C.S. Craun & T.H. Day. 1995. Heritability of a sexually selected character expressed in both sexes. Nature 374: 158–159.Google Scholar
  52. Williams, G.C. 1992. Natural selection: domains, levels, and challenges. Oxford University Press, Oxford. 208 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 1996

Authors and Affiliations

  • Alex Parker
    • 1
  • Irv Kornfield
    • 1
  1. 1.Department of Zoology and Center for Marine StudiesUniversity of MaineOronoU.S.A.

Personalised recommendations