Multigene phylogeny reveals eusociality evolved twice in vespid wasps

Abstract

Eusocial wasps of the family Vespidae are thought to have derived their social behavior from a common ancestor that had a rudimentary caste-containing social system. In support of this behavioral scenario, the leading phylogenetic hypothesis of Vespidae places the eusocial wasps (subfamilies Stenogastrinae, Polistinae, and Vespinae) as a derived monophyletic clade, thus implying a single origin of eusocial behavior. This perspective has shaped the investigation and interpretation of vespid social evolution for more than two decades. Here we report a phylogeny of Vespidae based on data from four nuclear gene fragments (18S and 28S ribosomal DNA, abdominal-A and RNA polymerase II) and representatives from all six extant subfamilies. In contrast to the current phylogenetic perspective, our results indicate two independent origins of vespid eusociality, once in the clade Polistinae+Vespinae and once in the Stenogastrinae. The stenogastrines appear as an early diverging clade distantly related to the vespines and polistines and thus evolved their distinctive form of social behavior from a different ancestor than that of Polistinae+Vespinae. These results support earlier views based on life history and behavior and have important implications for interpreting transitional stages in vespid social evolution.

Fig. 1.

Previous hypotheses of subfamily-level relationships of Vespidae. (A) The conventional hypothesis based on morphological and behavioral characters (4). (B) An alternative hypothesis based on limited molecular data (30), including the placement of Masarinae from a later study (36). Eusocial clades are indicated with gray shading.

Fig. 2.

Bayesian consensus phylogeny of all genes combined. Node support values are Bayesian posterior probabilities followed by ML bootstrap values on top and parsimony bootstrap followed by Bremer support values on the bottom. Clade values represented by NS are not supported for that analysis. Color-coded branches represent subfamilies, following the classificatory system of Carpenter (4). The eusocial clades are represented by gray shading.