Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches

Abstract

Despite more than half a century of research, the evolutionary origin of termites remains unresolved [1] [2] [3]. A clear picture of termite ancestry is crucial for understanding how these insects evolved eusociality, particularly because they lack the haplodiploid genetic system associated with eusocial evolution in bees, ants, wasps and thrips [4] [5]. Termites, together with cockroaches and praying mantids, constitute the order Dictyoptera, which has been the focus of numerous conflicting phylogenetic studies in recent decades [6] [7] [8] [9] [10] [11] [12]. With the aim of settling the debate over the sister-group of termites, we have determined the sequences of genes encoding 18S ribosomal RNA, mitochondrial cytochrome oxidase subunit II (COII) and endogenous endo-beta-1, 4-glucanase (EG) from a diverse range of dictyopterans. Maximum parsimony and likelihood analyses of these sequences revealed strong support for a clade consisting of termites and subsocial, wood-feeding cockroaches of the genus Cryptocercus. This clade is nested within a larger cockroach clade, implicating wood-feeding cockroaches as an evolutionary intermediate between primitive non-social taxa and eusocial termites.

The complete mitogenome of the wood-feeding cockroachCryptocercus kyebangensis(Blattodea: Cryptocercidae) and phylogenetic relations among cockroach families

“…Thus, these results strongly support the paraphyly of Blattodea in relation to termites, as suggested in other studies (e.g. Lo et al 2000;Pellens et al 2007;Legendre et al 2008;Cameron et al 2012;Djernaes et al 2012Djernaes et al , 2015. The current phylogenetic tree supports the sister relation of Blattidae and Blattellidae, with the clade Cryptocercidae + Isoptera as a sister group.…”

“…In addition, recent phylogenetic studies involving various mitochondrial or/and nuclear molecular markers showed that Cryptocercus is a sister group of a primitive termite species, Mastotermes darwiniensis (Lo et al 2000;Legendre et al 2008;Cameron et al 2012;Djernaes et al 2012). Because of these behavioral characteristics and their close relation with termites, wood-eating cockroaches of Cryptocercus have often been used as model species to elucidate the early stages of social evolution in termites (Klass et al 2008;Djernaes et al 2015).…”

Spirochete and protist symbionts of a termite ( Mastotermes electrodominicus ) in Miocene amber

“…These spirochetes belong to the family Pillotinaceae. Cryptocercus is considered an ancestral group to the termites (1,14,15). Images were produced by transmission electron microscopy.…”

“…astotermes, a genus of large tropical wood-ingesting termites, is of evolutionary importance for two reasons: (i) they harbor Mixotricha paradoxa and other amitochondriate many-genomed protists considered key to the early history of nucleated cells, and (ii) they are phylogenetically proximal to cockroaches (1). Both morphological and molecular features consistently place the single extant species (Mastotermes darwiniensis, family Mastotermitidae) as an early taxon ancestral to other termites.…”

Evolutionary trend of the small subunit nuclear ribosomal DNAs (SSU rDNAs) of wood-feedingCryptocercuscockroaches (Blattaria:Cryptocercus)

“…As references for comparative analysis of the aligned Cryptocercus sequences, we used previously published sequences of Mastotermes darwiniensis (AF220568; Genbank accession numbers) (Isoptera) (Lo et al 2000) and Tenodera aridifolia (AF423805) (Mantodea) (Whiting 2002) closely related to the genus Cryptocercus and that of Locusta migratoria (AF370793) (Orthoptera) (Giribet et al 2001) distantly related to the genus. We also used a previously published sequence of C. punctulatus species complex (AF220571) (Lo et al 2000) to compare with C. punctulatus species complex (MLBS).…”