Abstract
Subsocial wood feeding cockroaches in the genus Cryptocercus, the sister group of termites, retain their symbiotic gut flagellates during the host molting cycle, but in lower termites, closely related flagellates die prior to host ecdysis. Although the prevalent view is that termite flagellates die because of conditions of starvation and desiccation in the gut during the host molting cycle, the work of L.R. Cleveland in the 1930s through the 1960s provides a strong alternate hypothesis: it was the changed hormonal environment associated with the origin of eusociality and its concomitant shift in termite developmental ontogeny that instigates the death of the flagellates in termites. Although the research on termite gut microbial communities has exploded since the advent of modern molecular techniques, the role of the host hormonal environment on the life cycle of its gut flagellates has been neglected. Here Cleveland’s studies are revisited to provide a basis for re-examination of the problem, and the results framed in the context of two alternate hypotheses: the flagellate symbionts are victims of the change in host social status, or the flagellates have become incorporated into the life cycle of the eusocial termite colony. Recent work on parasitic protists suggests clear paths for exploring these hypotheses and for resolving long standing issues regarding sexual-encystment cycles in flagellates of the Cryptocercus-termite lineage using molecular methodologies, bringing the problem into the modern era.
Highlights
Overwhelming evidence is available from morphological characters and genomic analyses of both hosts and symbionts that termites are a clade nested within the cockroaches, with the wood-feeding, subsocial cockroach Cryptocercus as their undisputed sister group [2,3,4,5]
A prominent feature uniting Cryptocercus with the termites is a symbiotic relationship with single-celled anaerobic eukaryotes living in the enlarged hindgut paunch of the insects. These gut protists fall into two main groups traditionally known as flagellates—the Phylum Parabasalia and the Order Oxymonadida (Phylum Preaxostyla) [6], with the former historically divided into the trichomonads and hypermastigotes
A re-examination of this symbiotic relationship during host molt is overdue for two compelling reasons: first, because the need to re-acquire the symbiosis after molt precludes independent living by termite individuals, and second, because current literature rarely describes the symbiotic relationship during the host molting cycle in either insect taxon accurately
Summary
Overwhelming evidence is available from morphological characters and genomic analyses of both hosts and symbionts that termites are a clade nested within the cockroaches, with the wood-feeding, subsocial cockroach Cryptocercus as their undisputed sister group [2,3,4,5]. The protists are housed in the gut of an individual insect, living within a family (Cryptocercus) or colony (termites), which is lodged within the buffered environment of a nest They are supplied with a steady stream of food, in a liquid, temperature-controlled, safe haven. If the relationship of these two insect taxa to their gut fauna during developmental ontogeny is compared, it is obvious that there has been an evolutionary change during the host molting cycle In both Cryptocercus and lower termites, neonates acquire the flagellates from a parent or a sibling (the latter in established colonies of termites); the symbiosis is established at about the third instar in both taxa. This paper is an attempt to explore the foundations of that evolutionary transition
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