Patterns of genetic differentiation across three levels of intimate trophic relationships reveals evidence of strong reproductive isolation and host generalism in an inquiline wasp

Sequential divergence of inquilines with their hosts is an important subject of investigation for evolutionary biologists. While such coevolution is documented in some taxa, there are valid ecological and evolutionary reasons why inquilines might retain host flexibility rather than being restricted to specific hosts. The genus Synergus (Hymenoptera: Cynipidae) is an exclusively inquiline lineage of cynipid wasps associated with gall formers targeting plants of the family Fagaceae. In the southeastern US, the cynipid wasp genus Belonocnema (Hymenoptera: Cynipidae) are specialist gall formers on live oaks (Section Virentes) of the genus Quercus and targeted by many parasitoids and inquilines, including Synergus spp. Here we asked whether inquilines of the genus Synergus showed a corresponding population genomic structure with B. treatae lineages and/or its host's corresponding host plant species. Galls of B. treatae were collected from three live oak species at sites across their US ranges, extending from south central Texas, along the Gulf Coast to south Florida and up the Atlantic coast to North Carolina and Synergus individuals reared from galls. Employing a genotype-by-sequencing approach on 757 individuals, 17421 SNPs were used to evaluate population genomic structure using ENTROPY. Population genomic analyses suggest at least five distinct lineages of Synergus, all of which appear to show little to no admixture. Results show no clear associations of Synergus lineages with Belanocnema lineages or their live oak host plant species. This research illustrates the importance of ecological and evolutionary factors other than those often considered most significant as selection pressures on inquilines.