Flagellates Cause Eusociality

Hindgut protozoans were crucial in the evolution of eu-sociality 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; Anders-son, 1984). Moreover, the bulk of evidence suggests that protozoan loss at molt in termites did not precede euso-ciality. It is a secondary condition derived from eusocial-ity 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 in-traspecific 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 (Grasse and Noi-

rot, 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 euso-ciality, then, is not supported. The interdependence that the condition enforces on hosts nonetheless played a key role after the initial transition from subsociality to euso-ciality (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" (Holldobbler and Wilson, 2005), when individuals became incapable of a solitary existence.

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