Describing biodiversity in the genomics era: A new species of Nearctic Cynipidae gall wasp and its genome

Abstract

Gall wasps (Hymenoptera: Cynipidae) specializing on live oaks in the genus Quercus (subsection Virentes) are a relatively diverse and well‐studied community with 14 species described to date, albeit with incomplete information on their biology, life history and genetic structure. Incorporating an integrative taxonomic approach, we combine morphology, phenology, behaviour, genetics and genomics to describe a new species, Neuroterus valhalla sp. nov. The alternating generations of this species induce galls on the catkins and stem nodes of Quercus virginiana and Quercus geminata in the southern United States. We describe both generations in the species' life cycle, and primarily use samples from a population in the centre of Houston, Texas, thus serving as an example of the undescribed biodiversity still present in well‐travelled urban centres. In parallel, we present a draft assembly of the N. valhalla genome providing a direct link between the type specimen and reference genome. The genome of N. valhalla is the smallest reported to date within the tribe Cynipini, providing an important comparative contrast to the otherwise large genome size of cynipids. While relatively small, the genome was found to be composed of >64% repetitive elements, including 43% unclassified repeats and 11% retrotransposons. A preliminary ab initio and homology‐based annotation revealed 32,005 genes, and a subsequent orthogroup analysis grouped 18,044 of these to 8186 orthogroups, with some evidence for high levels of gene duplications within Cynipidae. A mitochondrial barcode phylogeny linked each generation of the new species and a phylogenomic ultraconserved element (UCEs) phylogeny indicates that the new species groups with other Nearctic Neuroterus. However, both phylogenies present the genus Neuroterus in North America as polyphyletic.

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

“…As in several previous phylogenetic treatments of the Cynipini (Rokas et al 2003, Ács et al 2010, Ronquist et al 2015, Cooke 2018, Andersen et al 2021, Brandão-Dias et al 2022, several gall wasp genera, including Andricus, Callirhytis, Neuroterus, and Dryocosmus, were found to be either para-or polyphyletic in our tree topologies (Figures 1-4). Of the genera represented in the tree by more than three species, only three genera: Amphibolips, Acraspis, and Disholcaspis maintain monophyly, the latter only because of a recent revision (Melika et al 2021a) after Cooke (2018) had found Disholcaspis to be polyphyletic.…”

“…Most recently, Brandão-Dias et al (2022) added additional data harvested from published Cynipini genomes to expand the Blaimer et al (2020) UCE gall wasp dataset. Though not the main focus of any of these studies, in all cases the resultant phylogenies appear to show the Palearctic fauna as being paraphyletic.…”

“…Next, Blaimer et al (2020) sequenced some Cynipini as part of a larger study of Cynipoidea and found a likely point of origin for oak galling approximately ~50 MYA, roughly coincident with the split between subgenus Cerris and subgenus Quercus oaks (Hipp et al 2018). Most recently, Brandão-Dias et al (2022) added additional data harvested from published Cynipini genomes to expand the Blaimer et al (2020) UCE gall wasp dataset. Though not the main focus of any of these studies, in all cases the resultant phylogenies appear to show the Palearctic fauna as being paraphyletic.…”

“…We sequence UCEs for 86 species reared from galls collected from 24 species of oak across the continental United States. We paired these with existing UCE data from Palearctic and other Nearctic oak gall wasps (Blaimer et al 2020, Brandão-Dias et al 2022), such that our set spanned six of the eight oak sections and 11 of the 13 subsections of oak sections Lobatae and Quercus . Combining our new collections with existing Palearctic data allow us to re-contextualize relationships among the Nearctic and Palearctic Cynipini.…”

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data

“…2010, 2018). Rapid development and increased availability of tools designed to capture genomic DNA has led to increased use of genome-wide approaches to analysis of phylogenomics, biogeography, demography, host shifts, and tritrophic interactions of gall communities (Blaimer et al, 2020;Brandão-Dias et al, 2022, Bunnefeld et al, 2018Driscoe et al, 2019;Samacá-Sáenz et al, 2020;Walton et al, 2021;Zhang Y.M. et al, 2020).…”