Extraordinarily precise nematode sex ratios: Adaptive responses to vanishingly rare mating options

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 twelve 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. In contrast, in both nematode genera, only sexually undifferentiated juveniles disperse, and their mating pools routinely consist of eight or fewer adults. Across all mating pool sizes, the sex ratios observed in both nematode genera are consistently female-biased (~0.34 males), which is markedly less female-biased than is often observed in the host wasps (~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.

Evolutionary bet-hedging in structured populations

As ecosystems evolve, species can become extinct due to fluctuations in the environment. This leads to the evolutionary adaption known as bet-hedging, where species hedge against these fluctuations to reduce their likelihood of extinction. Environmental variation can be either within or between generations. Previous work has shown that selection for bet-hedging against within-generational variation should not occur in large populations. However, this work has been limited by assumptions of well-mixed populations, whereas real populations usually have some degree of structure. Using the framework of evolutionary graph theory, we show that through adding competition structure to the population, within-generational variation can have a significant impact on the evolutionary process for any population size. This complements research using subdivided populations, which suggests that within-generational variation is important when local population sizes are small. Together, these conclusions provide evidence to support observations by some ecologists that are contrary to the widely held view that only between-generational environmental variation has an impact on natural selection. This provides theoretical justification for further empirical study into this largely unexplored area.

Patterns of intraspecific morphological variability in soil mites reflect their dispersal ability

The ability to disperse is one of the most important factors influencing the biogeography of species and speciation processes. Highly mobile species have been shown to lack geographic population structures, whereas less mobile species show genetically strongly subdivided populations which are expected to also display at least subtle phenotypic differences. Geometric morphometric methods (GMM) were now used to analyze morphological differences between European populations of a presumed non-phoretic, little mobile mite species in comparison to a highly mobile, phoretic species. The non-phoretic species Scutacarus carinthiacus showed a phenotypic population structure, whereas the phoretic species S. acarorum displayed homogeneity. These different patterns most probably can be explained by different levels of gene flow due to different dispersal abilities of the two species. GMM proved to be a sensitive tool that is especially recommendable for the analysis of (old) museum material and/or specimens in microscopic slides, which are not suitable for molecular genetic analysis.

Consistent scaling of inbreeding depression in space and time in a house sparrow metapopulation

Inbreeding may increase the extinction risk of small populations. Yet, studies using modern genomic tools to investigate inbreeding depression in nature have been limited to single populations, and little is known about the dynamics of inbreeding depression in subdivided populations over time. Natural populations often experience different environmental conditions and differ in demographic history and genetic composition, characteristics that can affect the severity of inbreeding depression. We utilized extensive long-term data on more than 3,100 individuals from eight islands in an insular house sparrow metapopulation to examine the generality of inbreeding effects. Using genomic estimates of realized inbreeding, we discovered that inbred individuals had lower survival probabilities and produced fewer recruiting offspring than noninbred individuals. Inbreeding depression, measured as the decline in fitness-related traits per unit inbreeding, did not vary appreciably among populations or with time. As a consequence, populations with more resident inbreeding (due to their demographic history) paid a higher total fitness cost, evidenced by a larger variance in fitness explained by inbreeding within these populations. Our results are in contrast to the idea that effects of inbreeding generally depend on ecological factors and genetic differences among populations, and expand the understanding of inbreeding depression in natural subdivided populations.

Sex allocation, inbreeding, and measures of population differentiation in hermaphroditic metapopulations

ABSTRACTSelection in inbreeding populations is expected to favour female-biased sex ratios in dioecious or gonochoristic species as a result of local mate competition, a prediction that finds strong support in populations in which females have control of the proportion of their sons versus daughters. Local mate competition due to inbreeding should also promote female-biased sex allocation in hermaphrodites, with reduced emphasis on the production of sperm or pollen relative to eggs, ovules or seeds. While inbreeding can be the direct result of the mating system in local populations, it can also result from demographic causes such as population turnover in metapopulations with frequent local extinction and recolonization. This effect of the turnover of demes has previously been analysed under the ‘haystack model’ for species with separate sexes. Here, we use quantitative genetic simulations to ask how population turnover affects the evolution of sex allocation in hermaphroditic metapopulations, and we assess the extent to which different genetic measures of inbreeding and population differentiation, especially FST and Jost’s D, predict the equilibrium sex allocation. We find that population turnover may dramatically enhance the female bias of hermaphroditic metapopulations, particularly where the inter-deme migration rate is low, even where local inbreeding, measured by FIS, is low or absent. In such situations, FST is a good predictor of the equilibrium sex allocation, and much better than Jost’s D. Our study extends predictions for sex allocation in subdivided populations that might experience population turnover to hermaphroditic species, and draws attention in general to the power of Wright’s hierarchical inbreeding statistics to predict the sex allocation in metapopulations at equilibrium.

Dispersal alters the nature and scope of sexually antagonistic variation

Intra-locus sexual conflict, or sexual antagonism, occurs when alleles have opposing fitness effects in the two sexes. Previous theory suggests that sexual antagonism is a driver of genetic variation by generating balancing selection. However, these studies assume that populations are well-mixed, neglecting the effects of spatial subdivision. Here we use mathematical modelling to show that limited dispersal can fundamentally change evolution at sexually antagonistic autosomal and X-linked loci due to inbreeding and sex-specific kin competition. We find that if the sexes disperse at different rates, kin competition within the philopatric sex biases intralocus conflict in favour of the more dispersive sex. Furthermore, kin competition diminishes the strength of balancing selection relative to genetic drift, reducing genetic variation in small subdivided populations. Meanwhile, by decreasing heterozygosity, inbreeding reduces the scope for sexually antagonistic polymorphism due to non-additive allelic effects, and this occurs to a greater extent on the X-chromosome than autosomes. Overall, our results demonstrate that spatial structure is an important factor in predicting where to expect sexually antagonistic alleles. We suggest that observed interspecific and intragenomic variation in sexual antagonism may be explained by sex-specific dispersal ecology and demography.