EVOLUTION OF THE NUMBER OF SEXES

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Abstract
In sexually reproducing isogamous organisms, gametes (or diploid cells in ciliates) are classified into two or more groups called sexes, and mating occurs only between cells of different sexes. We have studied the evolutionary stability of the number of sexes maintained in a population by examining population-genetic models. For models in which the diploid genome determines the sex of conjugal cells, a one-locus system with three alleles of pecking-order dominance is assumed. Unlike traditional bisexual models, the genetic dynamics then depend on a rule, called mating kinetics, which determines the proportion of matings between each pair of sexes for given proportions of cells of the three sexes. The evolutionary consequences greatly depend on the mating kinetics assumed. Of the four mating kinetics examined, two give a large advantage to rare sexes whose cells quickly find heterosexual partners, which implies an evolutionary increase in the number of sexes. In contrast, the other two mating kinetics, in which gametes wait for suitable mates without being eliminated from the gamete pool during this waiting period, produce neutrally stable dynamics with curves or a surface of equilibria. Then random drift or differential fitness among sexes would result in the loss of sex alleles until only two remain in the population. This suggests a turnover of sexes; a new sex invades and replaces resident sexes after temporary coexistence. Similar results are obtained in models with haploid sex-determination and with autogamy. These two processes, however, may help to maintain many sexes indirectly by preventing the accumulation of recessive lethal mutations on sex chromosomes. The relationship of these models to models of self-sterility factors in plants and sex factors in honeybees is discussed. To summarize, the number of sexes should increase when conjugal cells must find mates during a limited period of time, otherwise a two-sex system should evolve. We conclude that there may be more isogamous species with three or more sexes than are currently known.
Funding Information
  • Special Project Research of Optimal Strategy and Social Structure
  • Ministry of Education, Science, and Culture of Japan