Revising the Superorganism: An Organizational Approach to Complex Eusociality

Abstract

Eusociality is broadly defined as: colonies consisting of overlapping generations, cooperative brood care, and a reproductive division of labor where sterile (or non-reproductive) workers help the reproductive members. Colonies of many complex eusocial insect species (e.g., ants, bees, termites) exhibit traits, at the collective level, that are more analogous to biological individuals rather than to groups. Indeed, due to this, colonies of the most complex species are typically a unit of selection, which has led many authors to once again apply the concept of the superorganism to eusocial insects. However, unlike Wheeler, who originally employed the concept from a physiological and evolutionary perspective, today the superorganism is typically understood only from an evolutionary perspective, using group selection. This is because of the widely held view that eusocial colonies are self-organized systems. According to this view, even the most complex eusocial systems can be explained by appealing to a set of local interactions between parts of an initially disordered system (i.e., self-organization), without the need of any hierarchical control. In this paper, we challenge the mainstream view that hierarchical control and regulation does not occur, or is not necessary, in complex eusocial colonies. Using a case study of honey bees (Apis mellifera), we develop an alternative to the self-organization approach that focuses on the hierarchical nature of the organization of complex eusocial systems-that we refer to as the hierarchical-organizational approach. In addition, we analyze how colonies of eusocial insects show a complex set of interactions between the different organisms that bring forth a new cohesive collective organization, and how in turn the constitutive entities of this collective organization are transformed in this process. This paper argues that an inter-identity (namely the superorganism) emerges at the collective level in complex eusocial colonies, such as honey bees, due to the hierarchically organized network of interactions within the colony.

Keywords: eusociality; hierarchical regulation; inter-identity; self-organization; superorganism.

Figure 1

Temporal polyethism. Worker bees, in A. mellifera, transition between the temporal worker castes, orange circles, as internal levels of juvenile hormone (JH) increase, represented as JH+. JH biosynthesis is affected by external factors, including inter-member signals: QPM, brood ester, E-β-ocimene, and ethyl oleate. QPM, brood ester, and ethyl oleate inhibit JH biosynthesis, flat-ended lines, and E-β-ocimene promotes JH biosynthesis, circle-ended line. The inter-member signals allow the ratio of the temporal worker castes to be controlled at the colony level, see text for more details. The timeline represents the typical age of workers in each caste in the active summer period.

Figure 2

Queen/worker production. Any fertilized egg can develop into a queen or worker in A. mellifera. The type of comb cell, orange squares, and diet, blue squares, determine the development of larvae. Large queen cells and royal jelly cause larvae from fertilized eggs to develop into queens, whereas small comb cells and brood food cause equivalent larvae to develop into workers. Royal jelly induces an epigenetic change within the larvae. The size of the comb cell constrains larval growth. See text for more details.