Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae

Abstract

Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all "lower" termites rely on cellulolytic protists to digest wood, "higher" termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by "lower" termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of "higher" termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.

Keywords: Bacteria; Fungi; Higher termites; Lower termites; Nutritional mutualism; Protists; Sociality; Symbiosis; Termitomyces.

Fig. 1

The appearance of certain innovative traits during the course of termite evolution. Phylogeny simplified from [28]

Fig. 2

Nest centre, including royal chamber, of the carton nest of Coptotermes gestroi, resulting from the reuse of faecal material, organic matter from the soil, and soil microbes (photo: T. Chouvenc)

Fig. 3

Simplified diversification of derived Neoisoptera from [28]. The loss of nutritional mutualistic protozoa marked the emergence of Termitidae. While all termites possess various degrees of mutualistic relationships with intestinal Bacteria and Archaea, this figure highlights the characteristic partners involved in their obligate mutualistic relationship for nutritional purposes, and their respective locations relative to the termite hindgut. Excluding the subfamilies Sphaerotermitinae and Macrotermitinae, most other Termitidae are soil feeders, with many instances of independent reversal to a wood-feeding diet

Fig. 4

Fungal comb of Macrotermes (photo: J. Šobotník)

Fig. 5

Scenario A: the externalization of the digestion hypothesis

Fig. 6

Carton material from a dead Coptotermes colony invaded by Leucocoprinus (as observed in [209])

Fig. 7

Scenario B: the soil-feeder (edaphophagy) hypothesis