Extraordinarily precise nematode sex ratios: adaptive responses to vanishingly rare mating opportunities.

Sex ratio theory predicts both mean sex ratio and variance under a range of population structures. Here, we compare two genera of phoretic nematodes (Parasitodiplogaster and Ficophagus spp.) associated with 12 fig pollinating wasp species in Panama. The host wasps exhibit classic local mate competition: only inseminated females disperse from natal figs, and their offspring form mating pools that consist of scores of the adult offspring contributed by one or a few foundress mothers. By contrast, in both nematode genera, only sexually undifferentiated juveniles disperse and their mating pools routinely consist of 10 or fewer adults. Across all mating pool sizes, the sex ratios observed in both nematode genera are consistently female-biased (approx. 0.34 males), but markedly less female-biased than is often observed in the host wasps (approx. 0.10 males). In further contrast with their hosts, variances in nematode sex ratios are also consistently precise (significantly less than binomial). The constraints associated with predictably small mating pools within highly subdivided populations appear to select for precise sex ratios that contribute both to the reproductive success of individual nematodes, and to the evolutionary persistence of nematode species. We suggest that some form of environmental sex determination underlies these precise sex ratios.

Fisher vs. the Worms: Extraordinary Sex Ratios in Nematodes and the Mechanisms that Produce Them.

Parker, Baker, and Smith provided the first robust theory explaining why anisogamy evolves in parallel in multicellular organisms. Anisogamy sets the stage for the emergence of separate sexes, and for another phenomenon with which Parker is associated: sperm competition. In outcrossing taxa with separate sexes, Fisher proposed that the sex ratio will tend towards unity in large, randomly mating populations due to a fitness advantage that accrues in individuals of the rarer sex. This creates a vast excess of sperm over that required to fertilize all available eggs, and intense competition as a result. However, small, inbred populations can experience selection for skewed sex ratios. This is widely appreciated in haplodiploid organisms, in which females can control the sex ratio behaviorally. In this review, we discuss recent research in nematodes that has characterized the mechanisms underlying highly skewed sex ratios in fully diploid systems. These include self-fertile hermaphroditism and the adaptive elimination of sperm competition factors, facultative parthenogenesis, non-Mendelian meiotic oddities involving the sex chromosomes, and environmental sex determination. By connecting sex ratio evolution and sperm biology in surprising ways, these phenomena link two "seminal" contributions of G. A. Parker.

Differential effects of nematode infection on pollinating and non-pollinating fig wasps: Can shared antagonism provide net benefits to a mutualism?

Species pairs that form mutualistic associations are also components of broader organismal community networks. These interaction networks have shaped the evolution of individual mutualisms through interspecific interactions ranging from secondarily mutualistic to intensely antagonistic. Our understanding of this complex context remains limited because characterizing the impacts of species interacting with focal mutualists is often difficult. How is the fitness of mutualists impacted by the co-occurring interactive network of community associates? We investigated this context using a model interaction network comprised of a fig and fig wasp mutualist, eight non-pollinating fig wasp (NPFW) antagonists/commensals and a nematode previously believed to be associated only with the pollinator wasp mutualist. Through repeated sampling and field observations, we characterized the ecological roles of these mutualist-associated organisms to identify key antagonists. We then investigated how potential nematode infection of NPFWs could impact wasp survival across key life stages and, in turn, inferred how this influences the fitness of the fig-pollinator mutualists. Unexpectedly, we found all Ficus petiolaris-associated NPFWs to be the targets for nematode infection, with infection levels sometimes exceeding that of pollinators. Experimental data collected for the most abundant NPFW species suggest that nematode infection significantly reduces their longevity. Further, comparisons of nematode loads for emerging and successfully arriving NPFWs suggest that infection severely limits their dispersal ability. Through these observations, we conclude that this infection could impact NPFWs more severely than either mutualistic partner, suggesting a novel role of density-dependent facultative mutualism between figs, pollinator wasps and the nematode. This antagonist-mediated suppression of other network antagonists may present an ecologically common mechanism through which antagonists can present net benefits for mutualists' fitness.