Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both

Abstract

Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ~1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae, primarily the oaks (genus Quercus; ~435 sp). The association of oak gall wasps with oaks is ancient (~50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified a strong signal of host plant shifting among oak gall wasps. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich and where oaks are more phylogenetically diverse. We collected 86 species of Nearctic oak gall wasps from 10 of the 14 major clades of Nearctic oaks and sequenced >1000 Ultra Conserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than the analysis of previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host-associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Though formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host-associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants.

The arthropod associates of 155 North American cynipid oak galls

“…Relationship to galler phylogeny. Synergus wasps were reared from gall types across most of the Nearctic gall wasp phylogeny (Ward et al 2022), with some exceptions. In only two cases were Synergus reared from gall types produced by gallers in the large clade that includes genera Melikaiella Pujade-Villar, Loxaulus Mayr, and most of the Neuroterus Hartig (Supplementary Figure 1; gallers #2-15 in Figure 1a).…”

“…Due to the large size of these collections and our intention to use many in various future projects, we have not yet made a full set of voucher specimens available for study. However, vouchers for many of our gall wasps, and for wasps in the genera Synergus , Ormyrus, and Sycophila are already available (Ward et al 2020, Sheikh et al 2022, Ward et al 2022, Zhang et al 2022) and we intend to make vouchers of other genera available as more publications emerge from this dataset. Researchers interested in this material sooner than vouchers are made available may contact authors AAF, SPE, or KMP.…”

“…We used a common treatment to this end: Some insect genera might be associated with a phylogenetically-limited subset of gall wasps, and, if so, such patterns might inform hypotheses about the ecology and evolution of those gall associates. Thus, we created a slightly modified version (Supplemental Figure 1) of a recently published North American gall wasp phylogeny (Ward et al 2022), and then mapped collection data for each member of the genus onto that tree. We also mapped historical records of collections onto the tree when those records were available (Gillette 1896; Krombein et al 1979; Bugbee 1967; Yoshimoto 1971; Hansen 1992; Noyes 2022).…”

“…Relationship to galler phylogeny. Ormyrus were reared in this study or previously reared by others from almost all gall types included in the Nearctic gall wasp phylogeny (Ward et al 2022) phylogeny, including from all four Palearctic clades (Figure 4a). Members of the genus are near ubiquitous in associations with oak gall wasps.…”

“…Three developments now position researchers working in North America to explore fundamental dimensions of gall-associated insect diversification and together raise the possibility that some gall- associated insects may have diversified either via co-speciation with gall wasps or by frequently shifting between different host galls. One, the publication of a robust phylogeny of North American Cynipid oak gallers (Ward et al 2022) now offers opportunities to contextualize insect gall associations across an evolutionary dimension. Two, several of the same insect natural enemy genera are known to be commonly reared from many different oak galls, and particular clades within each genus are known to specialize on oak galls (Gillette 1896, Balduf 1932, Grissell 1976, Hanson 1992, Lobato-Vila et al 2019).…”