Evidence for social parasitism of early insect societies by Cretaceous rove beetles

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.

Termitariophily: expanding the concept of termitophily in a physogastric rove beetle (Coleoptera: Staphylinidae)

“…It seems non-contentious that the earliest 'higher' group Aleocharinae beetles (which includes Corotocini) are from the Paleogene: Eocene, c. 45 million years ago (mya), whereas the earliest Termitidae termites (in which Nasutitermitinae: Constrictotermes are included), are from the transition between the Paleogene: Paleocene and the Paleogene: Eocene, c. 55 mya (Engel et al, 2009;Cai et al, 2017). Despite ongoing discussion regarding the actual timing of the onset of termitophily in the evolutionary history of Aleocharinae (Yamamoto et al, 2017), authors tend to agree that: (i) limuloid and physogastric morphs evolved independently; (ii) the limuloid morph appeared earlier, as an adaptation to living under tree barks and in leaf litter, being posteriorly co-opted for defence; and (iii) whereas limuloids are adapted to hide and avoid contacts with their hosts, physogastrics engage in frequent guest-host interactions (Kanao et al, 2016;Yamamoto et al, 2016;Cai et al, 2017).…”

“…Moreover, Corotocini, being part of the 'higher' Aleocharinae, would have a limuloid stock among their early ancestors (Yamamoto et al, 2016;Cai et al, 2017). Moreover, Corotocini, being part of the 'higher' Aleocharinae, would have a limuloid stock among their early ancestors (Yamamoto et al, 2016;Cai et al, 2017).…”

“…In spite of the disproportionate number of examples of termitophilic species among Staphylinidae: Aleocharinae, the evolution of this type of symbiosis in these beetles remains elusive (Kanao et al, 2016;Yamamoto et al, 2016;Cai et al, 2017;Yamamoto et al, 2017). Within Aleocharinae, the tribe Corotocini stands as the largest and most specialized tribe, originating in the Neotropics in close association with Termitidae: Nasutitermitinae termites (Seevers, 1957;Jacobson, 1985).…”

“…However, as termitophiles are also found among other branches of Aleocharinae lacking a full set of these traits, one cannot consider them as an exclusive precondition to termitophily. Moreover, Corotocini, being part of the 'higher' Aleocharinae, would have a limuloid stock among their early ancestors (Yamamoto et al, 2016;Cai et al, 2017). The limuloid body shape, in turn, seems to be an adaptation to living under tree barks and in leaf litter, being posteriorly coopted for defence in a termitophilic context (Kanao et al, 2016).…”

Hox-logic of body plan innovations for social symbiosis in rove beetles

“…Independent evolutionary origins of staphylinid social parasitism are nonrandomly distributed across the family, with most occurring in the Aleocharinae, the largest subfamily of ~16,000 described species (7,11,12,22). The myriad instances of aleocharine myrmecophily and termitophily have been posited to stem from a preadaptive body plan that predisposes free-living species to evolve a socially parasitic lifestyle (7,23).…”