Nieves-Aldrey, J. L. | bioRxiv Science

bioRxiv2022

The Chalcidoidea bush of life - a massive radiation blurred by mutational saturation

Capturing phylogenetic signal from a massive radiation can be daunting. The superfamily Chalcidoidea is an excellent example of a hyperdiverse group that has remained recalcitrant to phylogenetic resolution. Chalcidoidea are mostly parasitoid wasps that until now included 27 families, 87 subfamilies and as many as 500,000 estimated species. We combined 1007 exons obtained with Anchored Hybrid Enrichment with 1048 Ultra-Conserved Elements (UCEs) for 433 taxa including all extant families, over 95% of all subfamilies and 356 genera chosen to represent the vast diversity of the superfamily. Going back and forth between molecular results and our collective morphological and biological knowledge, we detected insidious bias driven by the saturation of nucleotide data and highlighted morphological convergences. Our final results are based on a concatenated analysis of the least saturated exons and UCE data sets (2054 loci, 284,106 sites). Our analyses support a sister relationship with Mymarommatoidea. Seven of the previously recognized families were not monophyletic, so foundations for a new classification are discussed. Biology appears potentially more informative than morphology, as illustrated by the elucidation of a clade of plant gall associates and a clade of taxa with planidial first-instar larvae. The phylogeny suggests a shift from smaller soft-bodied wasps to larger and more heavily sclerotized wasps. Deep divergences in Chalcidoidea coincide with an increase in insect families in the fossil record, and an early shift to phytophagy corresponds with the beginning of the "Angiosperm Terrestrial Revolution". Our dating analyses suggest a Middle Jurassic origin of 174 Ma (167.3-180.5 Ma) and a crown age of 162.2 Ma (153.9-169.8 Ma) for Chalcidoidea. During the Cretaceous, Chalcidoidea underwent a rapid radiation in southern Gondwana with subsequent dispersals to the Northern Hemisphere. This scenario is discussed with regard to knowledge about host taxa of chalcid wasps, their fossil record, and Earths paleogeographic history.

evolutionary biology↗

bioRxiv2022

Phylogenomic Analysis of Protein-Coding Genes Resolves Complex Gall Wasp Relationships

The phylogeny of gall wasps (Cynipidae) and their parasitic relatives has attracted considerable attention in recent years. The family is now widely recognized to fall into thirteen natural lineages, designated tribes, but the relationships among them have remained elusive. This has stymied any progress in understanding how cynipid gall inducers evolved from insect parasitoids, and what role inquilinism (development as a herbivore inside galls induced by other cynipids) might have played in this transition. A recent analysis of ultraconserved elements (UCEs) represents the first attempt at resolving these questions using phylogenomics. Here, we present the first analysis based on protein-coding sequences from genome and transcriptome assemblies. To address potential problems due to model misfit, we focus on models that accommodate site-specific amino-acid profiles and that are less sensitive than standard models to long-branch attraction. Our results show that the Cynipidae as previously circumscribed are not monophyletic. Specifically, the Paraulacini and a clade formed by Diplolepidini + Pediaspidini both fall outside a core clade (Cynipidae s. str.), which is more closely related to Figitidae. This result is robust to the exclusion of long-branch taxa that could potentially mislead the analysis, and it is consistent with the UCE analysis. Given this, we propose that the Cynipidae be divided into three families: the Paraulacidae, Diplolepididae and Cynipidae (s. str.). Our results suggest that the Eschatocerini are the sister group of the remaining Cynipidae (s. str.). Within the latter, our results are consistent with the UCE analysis but place two additional tribes: (1) the Aylacini (s. str.), more closely related to the oak gall wasps (Cynipini) and some of their inquilines (Ceroptresini) than to other herb gallers (Aulacideini and Phanacidini); and (2) the Qwaqwaiini, likely the sister group to Synergini (s. str.) + Rhoophilini. Several alternative scenarios for the evolution of cynipid life histories are compatible with the relationships suggested by our analysis, but all are complex and require multiple shifts between parasitoids, inquilines and gall inducers. Linking the different types of life-history transitions to specific genomic signatures may be one of the best ways of differentiating among these alternative scenarios. Our study represents the first step towards enabling such analyses.

evolutionary biology↗