Abstract

The evolution of eusociality in ants and termites propelled both insect groups to their modern ecological dominance. Yet, eusociality also fostered the evolution of social parasitism—an adverse symbiosis, in which the superorganismal colonies formed by these insects are infiltrated by a profusion of invertebrate species that target nest resources. Predominant among these are the aleocharine rove beetles (Staphylinidae), a vast and ecologically diverse subfamily with numerous morphologically and behaviourally specialized socially parasitic lineages. Here, we report a fossil aleocharine, Mesosymbion compactus gen. et sp. nov., in Burmese amber (∼99 million years old), displaying specialized anatomy that is a hallmark of social parasites. Mesosymbion coexisted in the Burmese palaeofauna with stem-group ants and termites that provide the earliest indications of eusociality in both insect groups. We infer that the advent of eusociality led automatically and unavoidably to selection for social parasitism. The antiquity and adaptive flexibility of aleocharines made them among the first organisms to engage in this type of symbiosis.

Highlights

  • The evolution of eusociality in ants and termites propelled both insect groups to their modern ecological dominance

  • Such taxa live as socially parasitic myrmecophiles or termitophiles—specialized guests that exploit nest resources, prey on the brood, and in some cases achieve social integration where they are accepted as nestmates[8,9,10,11,12]

  • Aleocharines have arguably been the most successful arthropod group at capitalizing on the ecological dominance of eusocial insects[4,12], with previous authors reasoning that some socially parasitic relationships within the subfamily are ancient, extending back to near the origins of termites and ants in the Mesozoic[8,10,16]. This antiquity has been inferred indirectly: social parasitism occurs in some primitive aleocharine lineages of presumed Mesozoic origin[10], and the conserved associations of certain aleocharine groups with the same ant or termite subfamily across broad, often pantropical zoogeographic ranges have been interpreted as arising from Pangaean or Gondwanan vicariance[8,9,10,16,17,18,19]

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Summary

Introduction

The evolution of eusociality in ants and termites propelled both insect groups to their modern ecological dominance. Eusociality fostered the evolution of social parasitism—an adverse symbiosis, in which the superorganismal colonies formed by these insects are infiltrated by a profusion of invertebrate species that target nest resources Predominant among these are the aleocharine rove beetles (Staphylinidae), a vast and ecologically diverse subfamily with numerous morphologically and behaviourally specialized socially parasitic lineages. While the subfamily is relatively common in Cenozoic deposits, the single Mesozoic (mid-Cretaceous) species far reported belongs to the entirely free-living, basal lineage of Aleocharinae[31], providing no insight into when the socially parasitic groups in the remainder of the subfamily might have arisen We address these uncertainties directly with a new and unusual aleocharine fossil in mid-Cretaceous Burmese amber, dated to 98.8 million years old (earliest Cenomanian)[32]. The new fossil taxon indicates that early colonies formed by these insects were targeted by specialized social parasites, extending the age of this kind of symbiosis back by B50 million years, close to the inferred advent of ant and termite eusociality

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