Breeding system evolution and sex ratio in Caenorhabditis

Abstract

Reproduction constitutes the principle determinant of organismal fitness and, therefore, a central theme in biology is devoted to understanding variation in the mode of reproduction and its effects within and among species. Different breeding systems lead to varying levels of inbreeding, outcrossing, and sex ratios---with concomitant effects on patterns of genetic variation, effective population size, and adaptation by natural selection. Theoretical studies have proposed many mechanisms to explain the diversity of breeding systems observed in nature, several models of which invoke deleterious effects of mutation as a dominant force in patterning breeding system evolution. These notions motivated the present investigations into (1) the factors contributing to outcrossing rates and sex ratio in Caenorhabditis elegans and their population genetic effects, and (2) the general importance of deleterious mutation in the evolution of breeding system, emphasizing the Caenorhabditis clade. Nematodes of the genus Caenorhabditis provide a convenient system for studying these issues because species vary in breeding system, self-fertile C. elegans hermaphrodites can be genetically transformed into females to create dioecious populations, and complete genomic sequences of two species allow genomic analysis. With this context, I constructed a quantitative model describing sex ratio and outcrossing as a function of male copulatory ability and sex-chromosome non-disjunction (as a consequence of the XO sex-determination mechanism). The sex ratio and amount of outcrossing in C. elegans were then predicted from laboratory experiments and nucleotide polymorphism data, by applying population genetic theory of selection at linked sites when partial selfing is taken into account. These analyses suggest that outcrossing occurs on the order of one percent. Subsequent computational and multigeneration experimental evolution studies of the potential influence of deleterious mutations on breeding system evolution demonstrated that (1) selfing species do not exhibit lower rates of deleterious mutation than outcrossing species, (2) a higher deleterious mutation rate does not prevent the invasion of selfing alleles into a population, and (3) adaptive modulation of sex-chromosome non-disjunction is unlikely to underlie the persistence of males in androdioecious species. These results indicate that mutational theories are unlikely to fully explain the evolution of breeding system and sex.