Ecology, evolution and division of labour in social insects

Caste and division of labour have formed the core of the study of the organization of insect societies for the past four decades. Indeed, the description and analysis of task allocation between colony members are fundamental to understanding the organization of a complex biological system whose functioning depends upon the behavioural integration of a potentially large number of individuals. Recent research has emphasized the dynamic nature and fluidity of task allocation (Gordon 1989, 1995), the role of self-organization (Page & Mitchell 1991) and the physiology and genetics of task partitioning (Page & Robinson 1991; Robinson 1992). The study of caste and division of labour, however, has historically been established in the evolution and ecology of social insects (Oster & Wilson 1978; Calabi & Traniello 1989; Holldobler & Wilson 1990; Schmid-Hempel 1992; Tschinkel 1993; Beshers & Traniello 1994). Although the basic tenets of caste theory were first formulated to explain the origin and significance of physical castes, caste theory has also provided a conceptual framework to examine the adaptiveness of age-based division of labour, although this aspect of caste theory has rarely been tested and is thus poorly understood (Schmid-Hempel 1992). The theory predicts that the behavioural characteristics of individuals, including worker behavioural development, have been shaped as part of the overall evolutionary design of a colony of a given species. As Holldobler & Wilson (1990, page 312) have stated, ‘Each species has its own distinctive pattern of temporal polyethism’. (In this commentary we consider the terms ‘age-based division of labour’ and ‘temporal polyethism’ to be interchangeable, and follow the definitions and usage of Oster & Wilson (1978) and Holldobler & Wilson (1990). We also believe that these terms and the social phenomena they describe adequately cover aspects of worker behavioural development and task performance flexibility, and therefore we prefer not to adopt Franks’ (1994) definition of temporal polyethism). The recent dialogue between Robinson et al. (1994) and Franks & Tofts (1994) provides a critical discussion of theoretical, genetic and physiological analyses of age-based division of labour; their debate on temporal polyethism relies on socially advanced hymenopteran species as model systems. The genetic and physiological approaches described by Robinson et al. (1994) focus on the mechanisms of polyethism and are relevant to the evolution and ecology of division of labour, because they detail the proximate basis of what appear to be adaptive patterns of behavioural development. Franks & Tofts (1994), in contrast, suggested that the behavioural schedules commonly identified as age polyethism emerge as a consequence of the rules workers follow in their search for tasks to perform in a colony. Specifically, they attempted to identify a simple regulatory process involving nest design and the spatial array of tasks to be carried out to explain polyethism (Tofts & Franks 1992; Sendova-Franks & Franks 1993; Franks & Tofts 1994; reviewed in Bourke & Franks 1995). Provocatively asserting that age polyethism ‘is a myth’ and that the relationship between age and task performance is not causal, Franks (1994) advocated a paradigm shift in the study of polyethism. We argue, as have other researchers, that patterns of division of labour in the social insects appear to be highly variable and species-specific. And, as has long been recognized, we acknowledge that division of labour may be related to the Correspondence: J. F. A. Traniello, Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, U.S.A. (email: jft@bio.bu.edu).