Frequency dependence in matings with water-borne sperm

A. J. Pemberton, Leslie Robert Noble, J. D. D. Bishop

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Negative frequency-dependent mating success - the rare male effect - is a potentially powerful evolutionary force, but disagreement exists as to whether previous work, focusing on copulating species, has robustly demonstrated this phenomenon. Noncopulating sessile organisms that release male gametes into the environment but retain their eggs for fertilization may routinely receive unequal mixtures of sperm. Although promiscuity seems unavoidable it does not follow that the resulting paternity obeys 'fair raffle' expectations. This study investigates frequency dependence in the mating of one such species, the colonial ascidian Diplosoma listerianum. In competition with an alternative sperm source males fathered more progeny if previously mated to a particular female than if no mating history existed. This suggests positive frequency-dependent selection, but may simply result from a mate order effect involving sperm storage. With fewer acclimation matings, separated by longer intervals, this pattern was not found. When, in a different experimental design, virgin females were given simultaneous mixtures of gametes at widely divergent concentrations, sperm at the lower frequency consistently achieved a greater than expected share of paternity - a rare male effect. A convincing argument as to why D. listerianum should favour rare sperm has not been identified, as sperm rarity is expected to correlate very poorly with ecological or genetic male characteristics in this pattern of mating. The existence of nongenetic female preferences at the level of colony modules, analogous in effect to fixed female preferences, is proposed. If visible to selection, indirect benefits from increasing the genetic diversity of a sibship appear the only likely explanation of the rare male effect in this system as the life history presents virtually no costs to multiple mating, and a near absence of direct (resource) benefits, whereas less controversial hypotheses of female promiscuity (e.g. trade up, genetic incompatibility) do not seem appropriate.

Original languageEnglish
Pages (from-to)289-301
Number of pages12
JournalJournal of Evolutionary Biology
Volume16
Issue number2
DOIs
Publication statusPublished - Mar 2003

Keywords

  • fixed female preference
  • frequency dependence
  • rare male
  • spermcast
  • ASCIDIAN DIPLOSOMA-LISTERIANUM
  • GENE FLOW
  • POECILIA-RETICULATA
  • SIMULTANEOUS HERMAPHRODITISM
  • BOTRYLLUS-SCHLOSSERI
  • MARINE INVERTEBRATE
  • SEXUAL REPRODUCTION
  • NATURAL-POPULATIONS
  • EXOGENOUS SPERM
  • FEMALE CONTROL

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