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

incipient colonies (Scharf et al., 2005). This supports the
idea that gut microbes may supply a metabolic boost at
crucial points in host life history.
Flagellates Cause Eusociality?
Hindgut protozoans were crucial in the evolution of eusociality
in their termite hosts, but not for the reasons
usually cited. In termites, the hindgut flagellates die just
prior to host ecdysis. A newly molted individual must
reestablish its symbiosis by proctodeal trophallaxis from
a donor nestmate, making group living mandatory. In the
classic literature, this codependence of colony members
was thought to be the main precondition for the evolution
of eusociality in termites; the idea can be traced to
the work of L.R. Cleveland (1934). While loss of flagellates
at molt may enforce proximity, it provides no
explanation for the defining characteristics of termite eusociality,
namely, brood care, overlapping worker generations,
and non-reproductive castes (Starr, 1979; Andersson,
1984). Moreover, the bulk of evidence suggests that
protozoan loss at molt in termites did not precede eusociality.
It is a secondary condition derived from eusociality
of the hosts, and is associated with the physiology of
developmental arrest and caste control (Nalepa, 1994).
Hindgut protozoans were crucial in the genesis of the
termite lineage, because an obligate symbiotic relationship
with them demands a reliable means of transmission
between generations. The life history characteristics of a
termite ancestor, as exemplified by Cryptocercus, combined
with the physiology of encystment of these particular
protozoans, mandate that this transmission could
only occur via proctodeal trophallaxis (Nalepa, 1994). In
an ancestor common to Cryptocercus and termites, flagellate
cysts were presumably passed to hatchlings by intraspecific
coprophagy in aggregations (Nalepa et al.,
2001a). The physiology of encystment in these protists,
however, does not allow for their transmission by adults.
Their encystment is triggered by the molting cycle of the
host; consequently they are passed in the feces only during
the developmental stages of nymphs. Cysts are never
found in the feces of adults or intermolts (Cleveland et al.,
1934; Cleveland and Nutting, 1955; Cleveland et al.,
1960). Cryptocercus is subsocial and semelparous. Most
adults spend their entire lives nurturing one set of offspring.
Consequently, older nymphs are not present in
galleries when adults reproduce (Seelinger and Seelinger,
1983; Nalepa, 1984; Park et al., 2002). Coprophagy as a
mechanism of intergenerational transmission is thus
ruled out; adults do not excrete cysts, and older nymphs
are absent from the social group. Cysts in the feces of
molting Cryptocercus nymphs, as well as vestiges of the
sexual/encystment process in termites (Grassé and Noirot,
1945; Cleveland, 1965; Messer and Lee, 1989), are a
legacy of their distant gregarious past. In the ancestor
Cryptocercus shared with termites, an obligate relationship
with gut symbionts, intergenerational transmission
via proctodeal trophallaxis, and subsociality were thus a
co-evolved character set (Nalepa, 1991; Nalepa et al.,
2001a). Proctodeal trophallaxis in young families of a
Cryptocercus-like ancestor assured not only passage of
cellulolytic flagellates between generations, but also passage
of the entire complex of microorganisms present in
the hindgut fluids. Trophallaxis thus conserved relationships
between microbial taxa within consortia, allowing
them to develop interdependent relationships by eliminating
redundant pathways. The metabolic efficiency
of these consortia consequently increased, shifting the
cost-benefit ratio in favor of increased host reliance. The
growing dependence of the host on gut microbes, in turn,
reinforced selection for assured passage between generations
via subsociality and trophallactic behavior. The
switch from horizontal to vertical intergenerational
transmission of gut fauna was thus one of the key influences
in the transition from gregarious to subsocial behavior
in the common ancestor of Cryptocercus and termites.
It also set up one of the pivotal conditions allowing
for the transition to eusociality by establishing the behavioral
basis of trophallactic exchanges (Nalepa et al.,
2001a).
The hypothesis that the loss of protozoan symbionts at
molt was influential during the initial transition to eusociality,
then, is not supported. The interdependence that
the condition enforces on hosts nonetheless played a key
role after the initial transition from subsociality to eusociality
(detailed below). Subsequent hormonal changes
related to developmental stasis and caste evolution, and
the associated loss of protozoans at molt resulted in a
“point of no return” (Hölldobbler and Wilson, 2005),
when individuals became incapable of a solitary existence.
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.
Grassé 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
160 COCKROACHES