Evolutionary biologists have long been interested in understanding the mechanisms underlying Haldane's rule. The explanatory theories of dominance and faster-X, which are based on recessive alleles being expressed in the heterogametic sex, have been proposed as common mechanisms. These mechanisms predict that greater hemizygosity leads to both faster evolution and greater expression of intrinsic postzygotic isolation. Under these mechanisms, haplodiploids should evolve and express intrinsic postzygotic isolation faster than diploids because the entire genome is analogous to a sex chromosome. Here, we measure sterility and inviability in hybrids between Neodiprion pinetum and N. lecontei, a pair of haplodiplopids that differ morphologically, behaviorally, and genetically. We compare the observed isolation to that expected from published estimates of isolation in diploids at comparable levels of genetic divergence. We find that both male and female hybrids are viable and fertile, which is less isolation than expected. We then discuss several potential explanations for this surprising lack of isolation, including alternative mechanisms for Haldane's rule and a frequently overlooked quirk of haplodiploid genetics that may slow the emergence of complete intrinsic postzygotic isolation in hybrid males. Finally, we describe how haplodiploids, an underutilized resource, can be used to differentiate between mechanisms of Haldane's rule.
Empirical data from diverse taxa indicate that the hemizygous portions of the genome (X/Z chromosomes) evolve more rapidly than their diploid counterparts. Faster-X theory predicts increased rates of adaptive substitutions between isolated species, yet little is known about species experiencing gene flow. Here we investigate how hemizygosity impacts genome-wide patterns of differentiation during adaptive divergence with gene flow, combining simulations under isolation-with-migration models, a meta-analysis of autosomes and sex-chromosomes from diverse taxa, and analysis of haplodiploid species. First, using deterministic and stochastic simulations, we show that elevated differentiation at hemizygous loci occurs when there is gene flow, irrespective of dominance. This faster-X adaptive differentiation stems from more efficient selection resulting in reduced probability of losing the beneficial allele, greater migration-selection threshold, greater allele frequency differences at equilibrium, and a faster time to equilibrium. Second, by simulating neutral variation linked to selected loci, we show that faster-X differentiation affects linked variation due to reduced opportunities for recombination between locally adaptive and maladaptive immigrant haplotypes. Third, after correcting for expected differences in effective population size, we find that most taxon pairs (24 out of 28) exhibit faster-X differentiation in the meta-analysis. Finally, using a novel approach combining demographic modeling and simulations, we found evidence for faster-X differentiation in haplodiploid pine-feeding hymenopteran species adapted to different host plants. Together, our results indicate that divergent selection with gene flow can lead to higher differentiation at selected and linked variation in hemizygous loci (i.e., faster-X adaptive differentiation), both in X/Z-chromosomes and haplodiploid species.
Evolutionary conflicts are pervasive in nature and have the potential to drive antagonistic coevolution of conflict-related traits. However, when such conflicts are weak or idiosyncratic, phenotypic signatures of coevolutionary arms races may be absent. Here, we ask whether variation in group-living traits among pine-sawfly species in the genus Neodiprion is consistent with a history of parent-offspring conflict. To address this question, we compile data on adult female clutch size, larval aggregation behavior, and larval group size for a monophyletic group of 19 eastern North American Neodiprion species from field observations, laboratory assays, and published descriptions. We then evaluate the extent to which each trait exhibits phylogenetic signal and, based on these results, examine correlations between group-size traits both with and without phylogenetic correction. Although female oviposition behavior and larval grouping behavior varies among species and variation in these traits is decoupled from phylogeny, we find no evidence of antagonistic coevolution between these traits. Furthermore, while larvae are physically capable of dispersal, female clutch size is a strong predictor of larval colony size, indicating that larvae do not substantially alter initial group size after hatching. Thus, although theoretical work demonstrates the potential for parent-offspring conflict over group size in animals that lack parental care, our data suggest that this type of conflict is not likely to be a long-term driver of phenotypic evolution.
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