Phylogenomics indicates Amazonia as the major source of Neotropical swarm-founding social wasp diversity

Abstract

The Neotropical realm harbours unparalleled species richness and hence has challenged biologists to explain the cause of its high biotic diversity. Empirical studies to shed light on the processes underlying biological diversification in the Neotropics are focused mainly on vertebrates and plants, with little attention to the hyperdiverse insect fauna. Here, we use phylogenomic data from ultraconserved element (UCE) loci to reconstruct for the first time the evolutionary history of Neotropical swarm-founding social wasps (Hymenoptera, Vespidae, Epiponini). Using maximum likelihood, Bayesian, and species tree approaches we recovered a highly resolved phylogeny for epiponine wasps. Additionally, we estimated divergence dates, diversification rates, and the biogeographic history for these insects in order to test whether the group followed a ‘museum’ (speciation events occurred gradually over many millions of years) or ‘cradle’ (lineages evolved rapidly over a short time period) model of diversification. The origin of many genera and all sampled extant Epiponini species occurred during the Miocene and Plio-Pleistocene. Moreover, we detected no major shifts in the estimated diversification rate during the evolutionary history of Epiponini, suggesting a relatively gradual accumulation of lineages with low extinction rates. Several lines of evidence suggest that the Amazonian region played a major role in the evolution of Epiponini wasps. This spatio-temporal diversification pattern, most likely concurrent with climatic and landscape changes in the Neotropics during the Miocene and Pliocene, establishes the Amazonian region as the major source of Neotropical swarm-founding social wasp diversity.

Marimbondos: systematics, biogeography, and evolution of social behaviour of neotropical swarm‐founding wasps (Hymenoptera: Vespidae: Epiponini)

“…However, analyses relying exclusively on morphological and behavioural data (Carpenter, 1991;Wenzel and Carpenter, 1994;da Silva et al, 2014) as well as microsatellite flanking sequences and mitochondrial COI (Ar evalo et al, 2004) show the relationship Polistini (Mischocyttarini (Ropalidiini (Epiponini))). Molecular data (Hines et al, 2007;Pickett and Carpenter, 2010;Piekarski et al, 2018;Menezes et al, 2020) point to a closer relationship between Epiponini and Polistini, as obtained in our analysis. From the point of view of the evolution of sociality, the positioning of Polistini is puzzling, because traditionally Polistes is considered a key taxon for the evolution of social behaviour, bearing most of the conditions that would lead to more complex societies (West-Eberhard, 1969).…”

“…2E). Lastly, Menezes et al (2020) proposed a phylogenomic hypothesis for Epiponini based on Ultra Conserved Elements data. The interpretation of Angiopolybia as the sister lineage of all remaining swarm-founding social wasps as well as other relationships recovered by Piekarski et al (2018) was confirmed, and a biogeographical scenario was proposed for Epiponini, highlighting the relevance of Amazonia to the diversification of the clade.…”

“…Despite three decades of progress in epiponine phylogenetics, the above results underline the persistent instability in the relationships among some genera of Epiponini. The addition of molecular characters has Wenzel (1993), (c) Wenzel and Carpenter (1994), (d) Pickett and Carpenter (2010), and (e) Piekarski et al (2018) and Menezes et al (2020).…”

“…In addition, the interesting phenotypic characters (caste evolution, nest architecture) have not yet been optimized on a tree definitively. For example, Menezes et al (2020) introduce their study by discussing the importance of such traits, but then lay them aside and provide no enlightenment based on phylogeny. We remedy that shortcoming here.…”

An integrative taxonomic and phylogenetic approach reveals a new Neotropical swarm-founding social wasp, Pseudopolybia cryptica sp. n. (Vespidae: Polistinae: Epiponini)

“…We used the morphological matrix provided by Andena et al (2007) with few modifications: we excluded the characters 2, 3, 13, 15, and 23, because they were not informative for our analysis, and adapted the character states of the characters 11, 17, and 21 (Supplementary Table S4). We used Agelaia pallipes (Olivier, 1792), Angiopolybia pallens (Lepeletier, 1836), and Apoica pallens (Fabricius, 1804) as outgroups based on previous phylogenetic studies (Andena et al 2007;Menezes et al 2020). Finally, we used the Jukes-Cantor type model for morphological data with ascertainment bias correction (MK+ASC) and calculated branch supports with 1000 replicates of ultrafast bootstrap approximation (UFboot) (Minh et al 2013) and SH-like approximate likelihood ratio test (SH-aLRT) (Guindon et al 2010) as implemented in the IQ-tree software.…”