Specialized Myrmecophily at the Ecological Dawn of Modern Ants

Abstract

Myrmecophiles--species that depend on ant societies--include some of the most morphologically and behaviorally specialized animals known. Remarkable adaptive characters enable these creatures to bypass fortress-like security, integrate into colony life, and exploit abundant resources and protection inside ant nests. Such innovations must result from intimate coevolution with hosts, but a scarcity of definitive fossil myrmecophiles obscures when and how this lifestyle arose. Here, we report the earliest known morphologically specialized and apparently obligate myrmecophile, in Early Eocene (∼ 52 million years old) Cambay amber from India. Protoclaviger trichodens gen. et sp. nov. is a stem-group member of Clavigeritae, a speciose supertribe of pselaphine rove beetles (Coleoptera: Staphylinidae) heavily modified for myrmecophily via reduced mouthparts for trophallaxis with worker ants, brush-like trichomes that exude appeasement compounds, and fusions of many body and antennal segments. Protoclaviger captures a transitional stage in the evolutionary development of this novel body plan, most evident in its still-distinct abdominal tergites. The Cambay paleobiota marks one of the first occurrences in the fossil record of a significant presence of modern ants. Protoclaviger reveals that sophisticated social parasites were nest intruders throughout, and probably before, the ascent of ants to ecological dominance, with ancient groups such as Clavigeritae primed to radiate as their hosts became increasingly ubiquitous.

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

“…The taxon lacks the physogastric (swollen) body form of some aleocharine termitophiles81017, or a myrmecoid (ant-like) body shape that is seen in army ant-associated groups91012. Evidence of glandular complexes or trichomes associated with production of appeasement compounds is also missing1215—this highly intimate form of social parasitism thus far dates to the Early Eocene, manifested in the trichome-bearing pselaphine Protoclaviger 27. Before this study, the earliest-known aleocharines with comparable morphology to Mesosymbion are in Miocene Dominican and Mexican ambers1626.…”

“…The probability of recovering fossil social parasites of these rare Mesozoic ants and termites is extremely small; myrmecophiles and termitophiles typically exist at densities orders of magnitude lower than their hosts10, and consequently, no socially parasitic aleocharines have been reported before the Miocene1626. Moreover, the earliest-known social parasite belonging to any arthropod group—the myrmecophile Protoclaviger trichodens Parker and Grimaldi, a pselaphine rove beetle—is known from the Early Eocene (∼52 Mya)27. Second, the precondition for the evolution of social parasitism is the existence of resource-rich nests that invite exploitation.…”

Community Sampling and Integrative Taxonomy Reveal New Species and Host Specificity in the Army Ant-Associated Beetle Genus Tetradonia (Coleoptera, Staphylinidae, Aleocharinae)

“…These guests, when regularly associated with, rather than merely accidentally present with ants, are known as myrmecophiles [4]. Estimates of myrmecophile diversity range from 10,000 to 100,000 arthropod species in over 100 families [5–7]. Given their diversity, the myrmecophiles in and around ant colonies provide a good opportunity to study the structure and determinants of complex host-symbiont communities [8].…”

Leaf beetles are ant-nest beetles: the curious life of the juvenile stages of case-bearers (Coleoptera, Chrysomelidae, Cryptocephalinae)

“…Recently, Parker and Grimaldi (2014) described the earliest known specialized myrmecophile, a rove beetle (Staphylinidae) that dates to the early Eocene (52 mya). This indicates that myrmecophily is an ancient evolutionary phenomenon.…”