Evolution of flexible biting in hyperdiverse parasitoid wasps.

Thomas Van De Kamp,Arnold H Staniczek,Elias Hamann,Daria Bajerlein,Rebecca Spiecker,Tilo Baumbach,Benjamin Eggs,Lars Krogmann,Lea Hagelstein,István Mikó,Petr Janšta,Tomáš Faragó

doi:10.1098/rspb.2021.2086

Abstract

One key event in insect evolution was the development of mandibles with two joints, which allowed powerful biting but restricted their movement to a single degree of freedom. These mandibles define the Dicondylia, which constitute over 99% of all extant insect species. It was common doctrine that the dicondylic articulation of chewing mandibles remained unaltered for more than 400 million years. We report highly modified mandibles overcoming the restrictions of a single degree of freedom and hypothesize their major role in insect diversification. These mandibles are defining features of parasitoid chalcid wasps, one of the most species-rich lineages of insects. The shift from powerful chewing to precise cutting likely facilitated adaptations to parasitize hosts hidden in hard substrates, which pose challenges to the emerging wasps. We reveal a crucial step in insect evolution and highlight the importance of comprehensive studies even of putatively well-known systems.

Highlights

A major evolutionary step was the development of dicondylic mandibles with an additional anterior articulation to the head capsule [7], leading to the Dicondylia, which traditionally comprise all insects except the bristletails (Archaeognatha) [8]
Within Dicondylia, secondary monocondyly is known from insects, whose mouthparts are transformed into stylets (e.g. Hemiptera) [9], but all groups with chewing mouthparts are considered dicondylic
In an undescribed species of parasitoid wasps, we discovered peculiar antler-like extensions on top of otherwise ordinary-looking chewing mandibles

Summary

Introduction

In terms of species numbers and morphological and ecological diversity, insects are by far the most diverse lineage of terrestrial organisms [1–3]. In an undescribed species of parasitoid wasps, we discovered peculiar antler-like extensions on top of otherwise ordinary-looking chewing mandibles (figure 1). These extensions correspond to forward-projecting processes on the face and potentially serve as a grasping tool. We analysed the functional morphology of the mandibles of this extraordinary specimen by synchrotron X-ray microtomography and found evidence for flexible mandibular movement, contradicting the current hypothesis of largely conserved mandibular articulations and musculature in chewing insects. To test whether flexible mandibular movement represents a singular evolutionary event or might play a larger role in parasitoid evolution, we analysed the occurrence of this type of mandible throughout Chalcidoidea and all major lineages of Hymenoptera and correlated the morphological characters with the most recent molecular phylogenies of Hymenoptera [25] and Chalcidoidea [24]

Results

Discussion

Methods

Findings

31. Douissard P-A et al 2012 A versatile indirect detector