Energetic basis of colonial living in social insects

Abstract

Understanding the ecology and evolution of insect societies requires greater knowledge of how sociality affects the performance of whole colonies. Metabolic scaling theory, based largely on the body mass scaling of metabolic rate, has successfully predicted many aspects of the physiology and life history of individual (or unitary) organisms. Here we show, using a diverse set of social insect species, that this same theory predicts the size dependence of basic features of the physiology (i.e., metabolic rate, reproductive allocation) and life history (i.e., survival, growth, and reproduction) of whole colonies. The similarity in the size dependence of these features in unitary organisms and whole colonies points to commonalities in functional organization. Thus, it raises an important question of how such evolutionary convergence could arise through the process of natural selection.

Fig. 1.

Relationship between B ₀-normalized metabolic rate and body mass for resting unitary organisms and active whole colonies. Data are plotted for 12 colonies (ants, termites, bees, and wasps; SI Text) and 391 unitary insects from ref. .

Fig. 2.

Mass dependence of biomass production rate and reproductive allocation for unitary organisms and whole colonies. (A) Relationship between B ₀-normalized biomass production rate and mass for unitary organisms and whole colonies. Data are plotted for 16 colonies (ants, termites, bees, and wasps; SI Text) and 35 species of unitary organisms (data from ref. 23). (B) Relationship between gonad mass and somatic tissue mass for unitary organisms and whole colonies. Data are plotted for 117 colonies (ants, termites, bees, and wasps) and 512 species of unitary organisms (SI Text).

Fig. 3.

Dimensionless ontogenetic growth curve. A plot of the dimensionless mass ratio over ontogeny, (m/M)^1/4 [equivalent to the worker number ratio (n/N)^1/4], versus dimensionless time, at/4N ^1/4 − ln[1 − (n ₀/N)^1/4], for a variety of colonies and unitary organisms. Data are plotted for 13 unitary species (data from ref. 7) and eight colonies (ants, termites, bees, and wasps; SI Text). Note that the line is not fitted to the whole-colony data.

Fig. 4.

Mass dependence for B ₀-normalized life span for unitary insects and whole colonies. Data are plotted for 38 colonies (ants, bees, and wasps) and 16 unitary insects (SI Text).