Termitophiles, symbionts that live in termite nests, include a wide range of morphologically and behaviorally specialized organisms. Complex adaptive mechanisms permit these animals to integrate into societies and to exploit their controlled physical conditions and plentiful resources, as well as to garner protection inside termite nests. An understanding of the early evolution of termitophily is challenging owing to a scarcity of fossil termitophiles, with all known reliable records occurring from the Miocene (approximately 19 million years ago [mya]) [1-6], and an equivocal termitophile belonging to the largely free-living Mesoporini from the mid-Cretaceous [7]. Here we report the oldest, morphologically specialized, and obligate termitophiles from mid-Cretaceous Burmese amber (99 mya). Cretotrichopsenius burmiticus gen. et sp. nov. belongs to Trichopseniini, a group of distinctive termitophilous aleocharine rove beetles, all of which possess specialized swollen or horseshoe-crab-shaped body plans. Cretotrichopsenius display the protective horseshoe-crab-shaped body form typical of many modern termitophiles, with concealed head and antennae and strong posteriorly directed abdominal setae. Cretotrichopsenius represent the earliest definitive termitophiles, shedding light on host associations in the early evolution of termite societies. The fossil reveals that ancient termite societies were quickly invaded by beetles and by multiple independent lineages of social parasites over the subsequent eons.

Termites (Isoptera) are among the most ecologically ubiquitous of terrestrial eusocial insects and provide an attractive environment for symbionts, which have evolved numerous times independently, and in lineages as diverse as millipedes and beetles. Previous studies reported the discovery of unequivocal termitophily in mid-Cretaceous amber from northern Myanmar, providing evidence that pushed the origin of termitophily back into the Mesozoic. Here we report the discovery of two more pieces of Cretaceous amber containing individuals of the trichopseniine rove beetle Cretotrichopsenius burmiticus Cai et al., 2017 (Staphylinidae: Aleocharinae: Trichopseniini) preserved together with their potential host termites, providing further evidence regarding the association between these two insect lineages. Two new termite species and genera are described as putative hosts for C. burmiticus: Arceotermes hospitis Engel & Jiang, gen. et sp. nov. and Tanytermitalis philetaerus Engel & Cai, gen. et sp. nov. Each is included in a new family, Arceotermitidae Engel, fam. nov. (type genus: Arceotermes Engel & Jiang, gen. nov.), and Tanytermitidae Engel, fam. nov. (type genus: Tanytermes Engel et al., 2007). In order to better characterize these two families the classification of lower Isoptera and clade Xylophagodea (= Cryptocercidae + Isoptera) is emended with the following new taxa: Idanotermitinae Engel, subfam. nov.; Melqartitermitidae Engel, fam. nov.; Mylacrotermitidae Engel, fam. nov.; Krishnatermitidae Engel, fam. nov.; Cosmotermitinae Engel, subfam. nov.; Hodotermopsinae Engel, subfam. nov.; Artisoptera Engel, minord. nov.; Cryptocercaptera Engel, infraord. nov. Lower termites were remarkably diverse during the mid-Cretaceous but declined in diversity considerably by the Palaeogene. The fossil rove beetle Cretotrichopsenius Cai et al., 2017 currently provides the earliest definitive evidence of termitophily and the complex association between rove beetles and termites.

Termitophily—the symbiosis of organisms with termite societies—has evolved a disproportionate number of times within the rove beetle subfamily Aleocharinae (Staphylinidae). Among aleocharine termitophiles, defensive (limuloid) and mimetic (physogastric & physothoracic) body forms have evolved convergently, but due to lack of a comprehensive aleocharine phylogeny, the context in which termitophily and associated adaptations evolve is unknown. We present the first example of a robust, morphology-based phylogenetic placement of an exclusively termitophilous tribe, the Termitohospitini. Termitohospitini is recovered to be nested within Myllaenini sensu nov, and sister to Myllaena (new synonymy). Furthermore, we also recovered the small tribe Masuriini nested within Myllaenini sensu nov (new status).Reconstructing ecological transitions within this clade, we present evidence that the stem lineage of Myllaenini sensu nov invaded intertidal marine habitats, the common ancestor for Myllaena + Termitohospitini then transitioned to freshwater riparian habitats, with Termitohospitini alone subsequently shifting to termitophily. We conclude that: (1) Termitohospitini was ancestrally a limuloid-bodied riparian inhabitant; (2) a limuloid form may have been pre-adaptive for defense against host attack during the evolution of termitophily; (3) the strongly tapered abdomen of an ancestral limuloid body was a constraint on the evolution of physogastry, leading to the emergence of the unusual physothoracic body form observed in termitohospitines that likely integrates these obligate termitophiles to life inside termite colonies.“one of the most astonishing spectacles in all natural history.” — Richard Dawkins