Parallel and Nonparallel Patterns of Genetic Co-Differentiation: Evidence for Host Associated Differentiation Among Trophic Levels of the Oak Gall Wasp System
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Populations of phytophagous insects whose life cycles are intimately related to their host plants can express host-associated differentiation (HAD) in the form of genetic divergence and/or RI isolation across alternative host plants. In this work, we ask if HAD cascades to higher trophic levels in parasitoids of an insect herbivore that expresses HAD. Belonocnema treatae (Hymenoptera: Cynipidae) induces galls on three species of live oak (Quercus) across the southern USA. Both HAD and geography structure genomic variation among host associated populations of B. treatae. The generalist inquiline parasitoid, Synergus sp. (Hymenoptera: Cynipidae) develops within B. treatae galls. Herein, we test the hypothesis of co-genetic divergence between the inquiline and its insect host and between the inquiline and the host plant on which it develops. Genotyping-by-sequencing was conducted for 758 Synergus from 35 populations selected to reflect known genomic structure of B. treatae across its host plants and geographic range. Population genomic structure of the inquiline based on 57,664 single nucleotide polymorphisms was then investigated using Principal Component Analysis and the hierarchical Bayesian model ENTROPY to assign individuals to genetic clusters and estimate admixture proportions. ENTROPY revealed significant substructure within Synergus sp. corresponding to five independent lineages, three of which represent cryptic taxa. The five lineages display various degrees of overlap with respect to both host plant and geography including a longitudinal division shared with the gall former but no strong evidence of shared HAD with their insect host or their host plant. Thus, while the herbivorous insect displays HAD its inquiline parasites do not.