Double Symbiosis The Role Of Bacteroids

A hindgut filled to capacity with a huge complex of interacting microbiota was not the only symbiotic association influential in the evolution of termite eusociality. Grasse and Noirot (1959) noted nearly a half-century ago that the two taxa bracketing the transition from cockroaches to termites share a unique double symbiosis: an association with cellulolytic flagellates in the hindgut, and endosymbiotic bacteria housed in the visceral fat body. Cryptocercus is the only cockroach that has the former symbiosis, which it shares with all lower termites, and

Fig. 9.7 Male and female dealate primary reproductives of Mastotermes darwiniensis. Photo by Kate Smith, CSIRO Division of Entomology.

Mastotermes (Fig. 9.7) is the only isopteran with the latter, which it shares with all examined Blattaria (Bandi et al., 1995; Lo et al., 2003a). Mastotermes has additional characters that ally the taxon with cockroaches, including a well-developed anal lobe in the hindwing and the packaging of eggs in an ootheca (Watson and Gay, 1991; Nalepa and Lenz, 2000; Deitz et al., 2003).

The bacteroid-uric acid circulation system was in place when termites evolved eusociality (Fig. 9.1), possibly allowing for the mobilization of urate-derived nitrogen from the fat body and its transfer among conspecifics via coprophagy and trophallaxis (Chapter 5). The endosym-biosis was subsequently lost in other termite lineages when these diverged from the Mastotermitidae (Bandi and Sacchi, 2000). Other termites sequester uric acid in the fat body, but without bacteroids, individuals lack the ability to mobilize it from storage. Stored reserves can only be used by colony members via cannibalism or necrophagy. Once ingested, the uric acid is broken down by uricolytic bacteria in the hindgut (Potrikus and Brez-nak, 1981; Slaytor and Chappell, 1994). Bacteroids were likely lost in most termites because two aspects of euso-cial behavior made fat body endosymbionts redundant. The recycling of dead, moribund, and sometimes living nestmates, combined with the constant flow of hindgut fluids among nestmates via trophallaxis, allowed uri-colytic gut bacteria to be a more cost-efficient option (Bandi and Sacchi, 2000). It is of note, then, that after eu-sociality evolved, the storage and circulation of uric acid and its breakdown products changed from one that oc curs primarily at the level of individual physiology to one that occurs at the colony level. It is also of interest that proctodeal trophallaxis, a behavior linked to the presence of the hindgut symbionts, may have been influential in the loss of the fat body endosymbionts.

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