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

duction was suspended as adults fed and otherwise cared
for their dependent neonates, as reproductive stasis occurs
in extant young termite families when adults are nurturing
their first set of offspring (reviewed by Nalepa,
1994). This suggests that, as in Cryptocercus, parental care
during colony initiation in the termite ancestor was
costly.
The crucial step, and one that occurs during the ontogeny
of extant termite colonies, is that older nymphs assume
responsibility for feeding and maintaining younger
siblings, relieving their parents of the cost of brood care
and allowing them to invest in additional offspring (Fig.
9.8B). All defining components of eusociality (Michener,
1969; Wilson, 1971) follow. First, relieved of her provisioning
duties, the female can redirect her reserves into
oogenesis, and the result is a second cohort that overlaps
with offspring produced during the first reproductive
burst. Second, the assumption of responsibility for
younger siblings by the oldest offspring in the family constitutes
brood care. Third, by trophallactically feeding
younger siblings, fourth instars are depleting reserves that
could have been channeled into their own development,
thus delaying their own maturation (Nalepa, 1988b,
1994). A single behavioral change, the switch from parental
to alloparental care, thus represents the pathway for
making a seamless transition between adaptive points, accounting
with great parsimony for the defining components
of the early stages of termite eusociality (Nalepa
1988b, 1994). A key life history characteristic in a Cryptocercus-like
termite ancestor would be the extraordinarily
extended developmental period the first workers face,
even prior to assuming brood care duties. Tacking an addition
developmental delay onto the half dozen or so
years these nymphs already require to reach reproductive
maturity may be a pittance when balanced against the additional
eggs their already reproductively competent
mother may be able to produce as a result of their alloparental
behavior. A preliminary mathematical model indicates
that when a key resource like nitrogen is scarce, the
costs of delayed reproduction in these first workers are
outweighed by the benefits accrued by their labor in the
colony (Higashi et al., 2000). 4 A cockroach-like developmental
plasticity supplied the physiological underpinnings
for the social shift, as high-demand metabolic
processes such as reproduction and development are
tightly modulated in response to nutritional status in
Blattaria. It is of particular interest, then, that in extant
termites (Reticulitermes) two hexamerin genes may signal
nutritional status and participate in the regulation of
caste polyphenism (Zhou et al., 2006).
4. Masahiko Higashi was tragically killed in a boating accident in
March 2000 (Bignell, 2000b) and never completed the study.
HETEROCHRONY REVISITED
The recognition that heterochronic processes play a fundamental
role in social adaptations is increasingly recognized
in birds and mammals (see references in Gariépy et
al., 2001; Lawton and Lawton, 1986) but to date changes
in developmental timing have not received the attention
they deserve in studies of social insect evolution. Heterochrony
is pervasive in termite evolution, and most aspects
of isopteran biology can be examined within that
framework (Nalepa and Bandi, 2000). The evolution of
the initial stages of termite eusociality from subsocial ancestors
described above is predicated on a behavioral heterochrony,
an alteration in the timing of the expression of
parental care (Nalepa, 1988b, 1994). Recently, behavioral
heterochrony has been recognized as a key mechanism in
hymenopteran social evolution as well (Linksvayer and
Wade, 2005). Behavioral heterochronies often precede
physiological changes, with the latter playing a subsequent
supportive role (e.g., Gariépy et al., 2001); behavior
changes first, developmental consequences follow.
Development in the first termite workers was suspended
as a result of the initial behavioral heterochrony in an ancestor,
and selection was then free to shape a suite of interrelated
juvenile characters, including allogrooming,
kin recognition, coprophagy, and aggregation behavior. It
has been noted that paedomorphic taxa frequently develop
heightened social complexity, because the reduced
aggression associated with juvenile appearance and demeanor
enhances social interactions (e.g., Lawton and
Lawton, 1986). After alloparental care became established
in an ancestor, termite evolution escalated as the social
environment, rather than the external environment, became
the primary source of stimuli in shaping developmental
trajectories (Nalepa and Bandi, 2000, Fig. 4).
Major events were the rise of the soldier caste, the polyphyletic
onset of an obligately sterile worker caste excluded
from the imaginal pathway (Roisin, 1994, 2000),
and the loss of gut flagellates at molt, making group living
mandatory. The evolution of permanently sterile
castes is outside the scope of this chapter. We do, however,
note two conditions among extant young cockroaches
that provide substructure for the genesis of polyphenism
and division of labor. First, the potential for caste evolution
would be stronger in an ancestor with a juvenile
physiology, because young cockroaches are subject to the
most powerful group effects. Social conditions during the
early instars of Diploptera punctata, for example, can irreversibly
fix future developmental trajectories (Holbrook
and Schal, 1998). Second, evidence is increasing
that the process of forming aggregations in cockroaches
is a self-organized behavior (Deneubourg et al., 2002;
Garnier et al., 2005; Jeanson et al., 2005). In eusocial in-
TERMITES AS SOCIAL COCKROACHES 163