Cockroache; Ecology, behavior & history - W.J. Bell

Fig. 9.6 Scanning electron micrographs of flagellates from the hindgut of Cryptocercus punctulatus.
(A) The hypermastigote Trichonympha sp., scale bar 25 m. (B) The oxymonad Saccinobaculus
sp., scale bar 5 m. Images courtesy of Kevin J. Carpenter and Patrick J. Keeling.
gens, and those capable of nitrogen fixation, as well as
bacteria that participate in the biosynthesis of volatile
fatty acids (Breznak et al., 1974; Breznak, 1982; Noirot,
1995).
The common possession of oxymonad and hypermastigid
hindgut flagellates in Cryptocercus and lower
termites (Fig. 9.6) is often a focal point in discussions of
the evolutionary origins of termites. These protozoans
are unusually large, making them good subjects for a variety
of experimental investigations; some in the gut of
Cryptocercus are 0.3 mm in length and visible to the unaided
eye (Cleveland et al., 1934). They are unusually intricate,
with singular morphological structures and a
complex of bacterial symbionts of their own (e.g., Noda
et al., 2006). They are unique; most are found nowhere in
nature but the hindguts of these two groups (Honigberg,
1970). Finally, and of most interest for termite evolutionary
biology, most are cellulolytic and interdependent with
their hosts. For many years these flagellates were thought
to be not only the sole mechanism by which dictyopteran
wood feeders digested cellulose, but also the proximate
cause of termite eusociality. Currently, however, neither
of these hypotheses is fully supported, despite misconceptions
that still abound in the literature.
Dependence on Flagellates for Cellulase?
All termites and all cockroaches examined to date produce
their own cellulases, which are distinct from and
unrelated to those produced by the hindgut flagellates
(Watanabe et al., 1998; Lo et al., 2000; Slaytor, 2000;
Tokuda et al., 2004). The common possession of a certain
family of cellulase genes (GHF9) in termites, cockroaches,
and crayfish suggest that these enzymes were established
in the Dictyopteran lineage long before flagellates
took up permanent residence in the hindguts of an
ancestor of the termite-Cryptocercus clade (references in
Lo et al., 2003b). At present, Cryptocercus and lower termites
are considered to have a dual composting system
(Nakashima et al., 2002; Ohkuma, 2003); cellulose is degraded
by the combined enzymes of the host and the
hindgut flagellates. Nonetheless, these hosts are dependent
on the staggeringly complex communities of mutually
interdependent co-evolved organisms from the Archaea,
Eubacteria, and Eucarya in their digestive systems.
The interactions of the microbes with each other and
with their hosts are still poorly understood; however, exciting
inroads are being made by the laboratories actively
studying them, and the field is advancing quickly (e.g.,
Tokuda et al., 2004, 2005; Inoue et al., 2005; Watanabe et
al., 2006). Products of cellulose degradation by gut protozoans
may indirectly benefit the insect host by providing
energy for anaerobic respiration and nitrogen fixation
in gut bacteria (Bignell, 2000a; Slaytor, 2000). A comparison
of gene expression profiles among castes of the termite
Reticulitermes flavipes suggests that cellulases produced
by the symbionts may be particularly important in
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