A Test of Haldane's Rule in Neodiprion Sawflies and Implications for the Evolution of Postzygotic Isolation in Haplodiploids

Haldane's rule-a pattern in which hybrid sterility or inviability is observed in the heterogametic sex of an interspecific cross-is one of the most widely obeyed rules in nature. Because inheritance patterns are similar for sex chromosomes and haplodiploid genomes, Haldane's rule may apply to haplodiploid taxa, predicting that haploid male hybrids will evolve sterility or inviability before diploid female hybrids. However, there are several genetic and evolutionary mechanisms that may reduce the tendency of haplodiploids to obey Haldane's rule. Currently, there are insufficient data from haplodiploids to determine how frequently they adhere to Haldane's rule. To help fill this gap, we crossed a pair of haplodiploid hymenopteran species (Neodiprion lecontei and Neodiprion pinetum) and evaluated the viability and fertility of female and male hybrids. Despite considerable divergence, we found no evidence of reduced fertility in hybrids of either sex, consistent with the hypothesis that hybrid sterility evolves slowly in haplodiploids. For viability, we found a pattern opposite to that of Haldane's rule: hybrid females, but not males, had reduced viability. This reduction was most pronounced in one direction of the cross, possibly due to a cytoplasmic-nuclear incompatibility. We also found evidence of extrinsic postzygotic isolation in hybrids of both sexes, raising the possibility that this form or reproductive isolation tends to emerge early in speciation in host-specialized insects. Our work emphasizes the need for more studies on reproductive isolation in haplodiploids, which are abundant in nature but underrepresented in the speciation literature.

Automated summary

Haldane’s rule is a widely observed pattern in nature, where hybrid sterility or inviability occurs in the heterogametic sex of interspecific crosses. This rule may also apply to haplodiploid taxa, where haploid male hybrids are predicted to evolve sterility or inviability before diploid female hybrids. However, there are genetic and evolutionary mechanisms that could reduce the tendency of haplodiploids to follow Haldane’s rule. To investigate this, we crossed two haplodiploid hymenopteran species and evaluated the viability and fertility of the resulting hybrids. Our findings suggest that hybrid sterility evolves slowly in haplodiploids, as there was no evidence of reduced fertility in the hybrids. Interestingly, we observed a pattern opposite to Haldane’s rule, where hybrid females had reduced viability but not hybrid males. This study highlights the need for more research on reproductive isolation in haplodiploids, which are abundant in nature but underrepresented in speciation literature.