The Evolution of Eusociality in Termites: A Haplodiploid Analogy?

Since Hamilton (1964) first demonstrated that kin selection could act on the haplodiploid genetics of the Hymenoptera to lead to the evolution of sterile castes, the equally social termites (Isoptera) have posed a serious problem to the kin selection theory of insect eusociality. In the termites both males and females are diploid and follow a typical X-Y chromosomal sex determination, so that the unusual coefficients of relatedness that are found in the Hymenoptera would not seem to apply. The prevalent current hypothesis is that termite usociality is a consequence of their dependence on symbiotic intestinal flagellates (Wilson 1971). As was first suggested by Cleveland (Cleveland et al. 1934), the symbiotic relationship between termites and their cellulose-digesting protozoans may necessitate colonial life. The protozoans are lost at each molt and reinoculation takes place via nutrient transfer among colony members. In itself, however, this requirement for coloniality would not predispose the termites to the evolution of sterile castes. Certainly many other colonial organisms exist that have not subsequently evolved separate castes for reproduction and offspring care. Hamilton (1972) has suggested another possible evolutionary path to termite sociality. If inbreeding is common, then the high level of genetic relatedness within colonies might lead to a high degree of cooperativeness among colony members. It is difficult to see how Hamilton's inbreeding theory could lead to sterile castes, however, since inbreeding increases the genetic correlation between parents and progeny to the same extent as it increases the relationship between full siblings. (Both additive genetic orrelations equal 2 (1 + F), where F is the coefficient of inbreeding.) No amount of inbreeding will cause siblings to be closer genetically than are parents to their offspring, and thus inbreeding would not alter any evolutionary tendency for workers to forego reproduction i order to rear siblings. Dawkins (1978) has speculated that the genes of the symbiotic intestinal flagellates may have taken control over the physiology and behavior of their termite hosts, yet he offered no comment on how the protozoans might benefit from eusocial behavior in the termites. It appears that a mechanism for the evolution of sterile castes in termites till must be sought. Whitney (1976) has pointed out that organisms with chromosomal sex determination are functionally haplodiploid with respect o the X chromosome. Therefore a tendency for like-sex sib directed altruism in the homogametic sex may be expected to evolve if a substantial fraction of the genome is sex linked. Recent cytogenetic studies of termites have revealed a system of translocations that effectively inks much of the genome to the sex chromosomes. Syren and Luykx (1977) reported that males of the termite species Incisitermes chwarzi are heterozygous for a series of translocations inseven to eight of the 16 chromosome