Christine A. Nalepa

The establishment of intracellular symbiosis in an ancestor of cockroaches and termites

All cockroaches examined so far have been found to harbour a bacterial endosymbiont in specialized cells of the fat body, whereas Mastotermes darwiniensis is the only termite currently known to intracellular symbiont. The localization and mode of transmission of these bacteria are surprisingly similar, but so far no data have been published on their phylogenetic relationships. To address this issue, molecular sequence data were obtained from the genes encoding the small subunit ribosomal RNA of the M. darwiniensis endosymbiont, and compared with those obtained from endosymbionts of seven species of cockroaches. Molecular phylogenetic analysis unambiguously placed all these bacteria among the flavobacteria-bacteroides, indicating that the endosymbiont of M. darwiniensis is the sister group to the cockroach endosymbionts examined. Additionally, nucleotide divergence between the endosymbionts appears to be congruent with the palaeontological data on the hosts’s evolution. These results support previous claims that the original infection occurred in an ancestor common to cockroaches and termites. A loss of endosymbionts should subsequently have occurred in all termite lineages, except that which gave rise to M. darwiniensis.

Colony composition, protozoan transfer and some life history characteristics of the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae)

SummaryAdult pairs of the woodroach Cryptocercus punctulatus were reported to be incapable of founding colonies independently because the presence of a recently molted juvenile was required to transfer encysted symbiotic gut protozoa to newly hatched roaches. Field and laboratory evidence presented here shows that adult pairs of C. punctulatus do found colonies and that juveniles are generally not present to provide neonates with protozoan cysts. Newly hatched nymphs acquire their intestinal symbionts by feeding on the anal fluids of the adult roaches, i.e., by proctodeal trophallaxis. Conditions other than a symbiotic association with protozoans may have contributed to the evolution of eusociality in termites (Isoptera).

Inheritance and diversification of symbiotic trichonymphid flagellates from a common ancestor of termites and the cockroach Cryptocercus

Cryptocercus cockroaches and lower termites harbour obligate, diverse and unique symbiotic cellulolytic flagellates in their hindgut that are considered critical in the development of social behaviour in their hosts. However, there has been controversy concerning the origin of these symbiotic flagellates. Here, molecular sequences encoding small subunit rRNA and glyceraldehyde-3-phosphate dehydrogenase were identified in the symbiotic flagellates of the order Trichonymphida (phylum Parabasalia) in the gut of Cryptocercus punctulatus and compared phylogenetically to the corresponding species in termites. In each of the monophyletic lineages that represent family-level groups in Trichonymphida, the symbionts of Cryptocercus were robustly sister to those of termites. Together with the recent evidence for the sister-group relationship of the host insects, this first comprehensive study comparing symbiont molecular phylogeny strongly suggests that a set of symbiotic flagellates representative of extant diversity was already established in an ancestor common to Cryptocercus and termites, was vertically transmitted to their offspring, and subsequently became diversified to distinct levels, depending on both the host and the symbiont lineages.

Characterizing the Ancestors: Paedomorphosis and Termite Evolution

The relationships among the three main lineages in the Dictyoptera are uncertain. Here we suggest that the tempo and mode of their evolution confound efforts to determine the phylogenetic relationships among termites, mantids, and cockroaches. First, fossil and molecular data each suggest that these taxa originated within a relatively short span of time during the Mesozoic. If so, the rapid divergence of lineages during early stages of dictyopteran evolution may have obscured our ability to resolve the pattern of branching events. Second, other evidence suggests that paedomorphosis played a central role in shaping the evolutionary trajectory of termites. Paedomorphic evolution is notorious for obscuring phylogenetic patterns, because (a) reductions and losses result in few morphological characters on which to base cladistic analysis, and (b) parallel loss of characters by developmental truncation obscures polarity, making it difficult to distinguish between paedomorphic and plesiomorphic traits. Moreover, with cockroaches as the reference group, heterochronic changes are evident in termite behavior and physiology, providing insight into the origin of isopteran traits such as a reliance on gut mutualists and elaborate polyphenism. Recognition of the connection between ontogeny and phylogeny in the Dictyoptera is essential to resolving some of the long standing issues regarding the phylogenetic origin and subsequent evolution of the included taxa.

Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach.

The relationship between xylophagous termites and the protists resident in their hindguts is a textbook example of symbiosis. The essential steps of lignocellulose degradation handled by these protists allow the host termites to thrive on a wood diet. There has never been a comprehensive analysis of lignocellulose degradation by protists, however, as it has proven difficult to establish these symbionts in pure culture. The trends in lignocellulose degradation during the evolution of the host lineage are also largely unknown. To clarify these points without any cultivation technique, we performed meta-expressed sequence tag (EST) analysis of cDNA libraries originating from symbiotic protistan communities in four termite species and a wood-feeding cockroach. Our results reveal the establishment of a degradation system with multiple enzymes at the ancestral stage of termite-protistan symbiosis, especially GHF5 and 7. According to our phylogenetic analyses, the enzymes comprising the protistan lignocellulose degradation system are coded not only by genes innate to the protists, but also genes acquired by the protists via lateral transfer from bacteria. This gives us a fresh perspective from which to understand the evolutionary dynamics of symbiosis.

Cost of parental care in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera: Cryptocercidae)

SummaryThe objective of this study was to measure the effect of parental care on the reproductive capabilities and survival of adult Cryptocercus punctulatus Scudder. Brood removal studies show that the long term parental care exhibited by this woodroach can exact a cost in terms of future reproduction by delaying a second reproductive episode. If C. punctulatus is used as a model of the ancestral state of the termites, changes in responsibility for care giving behavior can account for all the higher components of eusociality (overlap of worker generations, brood care by workers, non-reproductive castes) by shifting the cost of parental care from the adults to the oldest offspring.

Wood-feeding cockroaches as models for termite evolution (Insecta: Dictyoptera): Cryptocercus vs. Parasphaeria boleiriana

Isoptera are highly specialized cockroaches and are one of the few eusocial insect lineages. Cryptocercus cockroaches have appeared to many as ideal models for inference on the early evolution of termites, due to their possible phylogenetic relationship and several shared key attributes in life history. Recently, Pellens, Grandcolas, and colleagues have proposed the blaberid cockroach Parasphaeria boleiriana to be an alternative model for the early evolution in termites. We compare the usefulness of Cryptocercus and P. boleiriana as models for termite evolution. Cryptocercus and lower Isoptera (1) can both feed on comparatively recalcitrant wood, (2) have an obligate, rich and unique hypermastigid and oxymonadid fauna in the hindgut, (3) transfer these flagellates to the next generation by anal trophallaxis, (4) have social systems that involve long-lasting biparental care, and, finally, (5) are strongly suggested to be sister groups, so that the key attributes (1)-(4) appear to be homologous between the two taxa. On the other hand, P. boleiriana (1) feeds on soft, ephemeral wood sources, (2) shows no trace of the oxymonadid and hypermastigid hindgut fauna unique to Cryptocercus and lower Isoptera, nor does it have any other demonstrated obligate relationship with hindgut flagellates, (3) is likely to lack anal trophallaxis, (4) has only a short period of uniparental brood care, and (5) is phylogenetically remote from the Cryptocercus+Isoptera clade. These facts would argue against any reasonable usage of P. boleiriana as a model for the early evolution of Isoptera or even of the clade Cryptocercus+Isoptera. Cryptocercus thus remains an appropriate model-taxon-by-homology for early termite evolution. As compared to P. boleiriana, some other Blaberidae (such as the Panesthiinae Salganea) appear more useful as model-taxa-by-homoplasy for the early evolution of the Cryptocercus+Isoptera clade, as their brooding behavior is more elaborate than in P. boleiriana.

Save Isoptera: A comment on Inward et al.

A number of phylogenetic studies during the last decade have shown that termites—one of the main groups of eusocial insects—are a type of cockroach, whose closest living relative is the wood-feeding genus Cryptocercus (reviewed in [Klass & Meier (2006)][1] and [Inward et al. (2007)][2]). Inward

EVOLUTION OF MONOGAMY IN TERMITES

Two hypotheses have been proposed to explain the origin of lifetime monogamy in the Isoptera. The classic explanation is that (1) the male must be present to continually provide sperm for the vast number of eggs produced by the queen (Snyder, 1924: Brian, 1983). Thornhill & Alcock (1983) proposed that (2) synchrony in the availability of receptive females necessitates mate guarding; males subsequently gain if they improve the relative reproductive success of their sole partner.

Ancestral Transfer of Symbionts between Cockroaches and Termites: An Unlikely Scenario

Thorne’s (Proc.R. Soc. Load. B 241, 37 (1990)) studies of the laboratory behaviour of extant vvoodroaches (Cryptocercus) and termites (Zootermopsis) suggest that transfaunation of hindgut protozoans potentially could occur by aggression and consumption in the held. However, existing literature suggests no overlap in protozoan species composition for these two taxa. Furthermore, it is doubtful that transfaunation would occur in the solitary ancestral ‘term itoid’ and ‘roachoid’ lines proposed by Thorne: not only is it unlikely that such insects would encounter each other, but it is doubtful that they would show the degree of aggression exhibited by the termite soldiers in her study. Inheritance from an ancestor common to Cryptocercus and the lower termites remains the most logical explanation for the presence of the unique cellulolytic oxymonad, trichomonad and hypermastigote flagellates in these two groups.