The evolutionary history of division of labour

Abstract

Functional specialization, or division of labour (DOL), of parts within organisms and colonies is common in most multi-cellular, colonial and social organisms, but it is far from ubiquitous. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences can arise easily. These mechanisms cannot explain the many groups of colonial and social animals that exhibit no DOL despite up to 500 million years of evolution. Here, I propose a new hypothesis, based on a multi-level selection theory, which predicts that a reproductive DOL is required to evolve prior to subsequent functional specialization. I test this hypothesis using a dataset consisting of the type of DOL for living and extinct colonial and social animals. The frequency distribution of DOL and the sequence of its acquisition confirm that reproductive specialization evolves prior to functional specialization. A corollary of this hypothesis is observed in colonial, social and also within multi-cellular organisms; those species without a reproductive DOL have a smaller range of internal variation, in terms of the number of polymorphs or cell types, than species with a reproductive DOL.

Figure 1.

The influence of propagule size—the number of members that found a new colony—on the probability of forming a descendent colony of a particular phenotype. Monomorphic colonies have one beneficial morph whereas dimorphic colonies have an equal number of two morphs. In this figure, there are initially 50 members, 10 of which are detrimental to the colony. The probability of producing an offspring with at least one detrimental member is the same for both aggregates and approaches unity as the number of members in a propagule (propagule size) increases.

Figure 2.

A comparison of the relative timing of reproductive division of labour (DOL) and ‘other’ DOL derived from molecular phylogenies of extant colonial and social organisms and multi-cellular algae. Each point represents the time relative to the base of the tree for a phylogenetically independent origin of DOL. Groups that have evolved one type of DOL but not the other are plotted within the grey bars, but the relative time of the DOL these groups do posses is plotted. Groups with reproductive but not ‘other’ DOL plot along the top of the figure and groups with ‘other’ but not reproductive DOL would plot along the right margin. The number of independently evolved groups that are colonial or social, but without DOL of any kind is also shown in the top right dark grey box. The organisms included are hydrozoans, octocoralls, scleractinian corals, bryozoans, entoprocts, phoronids, hemichordates and tunicates, the hymenopteran groups of the Vespoidea, termites, mammals and green algae.

Figure 3.

Patterns of DOL for multi-cellular and colonial organisms. (a) The proportion of non-reproductive members plotted against polymorph types for colonial and social animals. (b) The mechanism of germ-cell formation (which estimates the proportion of non-reproductive members) plotted against the number of cell types in multi-cellular animals, plants, fungi and algae, as well as colonial algae, ciliates and bacteria. S, somatically derived; E, epigenetically derived; P, preformed.