Variation in rates of spontaneous male production within the nematode species Pristionchus pacificus supports an adaptive role for males and outcrossing

Abstract

Background: The nematode species Pristionchus pacificus has an androdioecious mating system in which populations consist of self-fertilizing hermaphrodites and relatively few males. The prevalence of males in such a system is likely to depend on the relative pros and cons of outcrossing. While outcrossing generates novel allelic combinations and can therefore increase adaptive potential, it may also disrupt the potentially beneficial consequences of repeated generations of selfing. These include purging of deleterious alleles, inheritance of co-adapted allele complexes, improved hermaphrodite fitness and increased population growth. Here we use experimental and population genetic approaches to test hypotheses relating to male production and outcrossing in laboratory and natural populations of P. pacificus sampled from the volcanic island of La Réunion. Results: We find a significant interaction between sampling locality and temperature treatment influencing rates of spontaneous male production in the laboratory. While strains isolated at higher altitude, cooler localities produce a higher proportion of male offspring at 25 °C relative to 20 or 15 °C, the reverse pattern is seen in strains isolated from warmer, low altitude localities. Linkage disequilibrium extends across long physical distances, but fails to approach levels reported for the partially selfing nematode species Caenorhabditis elegans. Finally, we find evidence for admixture between divergent genetic lineages. Conclusions: Elevated rates of laboratory male generation appear to occur under environmental conditions which differ from those experienced by populations in nature. Such elevated male generation may result in higher outcrossing rates, hence driving increased effective recombination and the creation of potentially adaptive novel allelic combinations. Patterns of linkage disequilibrium decay support selfing as the predominant reproductive strategy in P. pacificus. Finally, despite the potential for outcrossing depression, our results suggest admixture has occurred between distinct genetic lineages since their independent colonization of the island, suggesting outcrossing depression may not be uniform in this species.