Context-Dependent Reproductive Isolation: Host Plant Variability Drives Fitness of Hybrid Herbivores

The role of divergent selection between alternative environments in promoting reproductive isolation (RI) between lineages is well recognized. However, most studies view each divergent environment as homogenous, thereby overlooking the potential role within-environment variation plays in RI between differentiating lineages. Here, we test the importance of microenvironmental variation in RI by using individual trees of two host plants, each harboring locally adapted populations of the cynipid wasp Belonocnema treatae. We compared the fitness surrogate (survival) of offspring from hybrid crosses with resident crosses across individual trees on each of two primary host plants, Quercus virginiana and Q. geminata. We found evidence of weak hybrid inviability between host-associated lineages of B. treatae despite strong genomic differentiation. However, averaging across environments masked great variation in hybrid fitness on individual trees, where hybrids performed worse than, equal to, or better than residents. Thus, considering the environmental context of hybridization is critical to improving the predictability of divergence under variable selection.

Automated summary

Divergent selection between alternative environments plays a crucial role in reproductive isolation, but the importance of within-environment variation in differentiation between lineages has been overlooked. This study revealed weak hybrid inviability between host-associated lineages of B. treatae despite strong genomic differentiation, with great variation in hybrid fitness observed on individual trees. Considering the environmental context of hybridization is essential for predicting divergence under variable selection.