The nature of ant caste allometry

Organismal characteristics such as the relative size and shape of body parts often scale with body size. Such allometry is ubiquitous across the tree of life, but the mechanistic underpinnings and evolution of allometric scaling remain unclear (1, 2). Social insect queen and worker castes provide striking examples of allometry for caste traits. For example, honey bee queens weigh about twice as much as workers, but their ovaries have approximately 100 times more ovariole filaments (3). Social insect researchers have identified many cases where genotype affects caste fate and the allometric relationship between body size and caste traits (3–8). Genetic changes are also usually assumed to drive the evolution of strong interspecific differences in caste allometry (Fig. 1). However, the degree to which environmental factors influence the expression and evolution of caste allometry remains relatively unexplored. On the one hand, adult body size and caste traits are clearly plastic with respect to environmental inputs during development. But do allometric scaling relationships themselves also depend on environmental factors, as has been found in other organisms (2)?

Fig. 1.

The clonal raider ant Oocerae biroi (Left) has no queens, but intercastes are on average about 10% larger than workers, have four ovarioles instead of two, and have vestigial eyes. In PNAS, Piekarski et al. (9) show that the allometric scaling relationships between body size and caste traits in O. biroi varies by clonal genotype but is robust to variation in rearing environment. Other related ants, such as the army ant Neivamyrmex opacithorax (Right), have striking queen–worker dimorphism, where queens are much larger than workers and have many hundreds of ovarioles (10). Caste allometry is also very likely to depend on genotype in ants such as N. opacithorax and may also strongly depend on environmental factors. Image credit: Drawings of O. biroi and N. opacithorax by Sachin Suresh (Arizona State University, Tempe, AZ).

In PNAS, Piekarski et al. (9) tested the degree to which the allometric scaling relationships between body size and caste-related traits depend on genotype and rearing environment in the queenless clonal raider ant Ooceraea biroi. The “hourglass model” developed by Trible and Kronauer for ant caste (11, 12) hypothesizes that various environmental and genetic factors influence a larva’s final body size, which determines the individual’s caste fate. Molecular factors tightly correlated with body size are hypothesized to subsequently determine caste-related traits such as ovary size and body shape. According to this model, all caste traits and body size are tightly integrated, and environmental factors can only affect caste traits via their impacts on body size (11, 12). As a result, caste allometry is predicted to be insensitive to variation in environmental factors. In contrast, the “standard model” developed for social insects more generally in previous literature (13–15) emphasizes modularity for each caste, so that queen and worker developmental trajectories can be decoupled to some degree, and queen and worker caste traits can evolve independently. Under such a model, genetic and environmental factors might affect the traits of each caste separately.

The clonal raider ant used by Piekarski et al. (9) does not have queens, but approximately one third of individuals in the studied strains and conditions are considered “intercastes” (Fig. 1). Regular workers and intercastes have overlapping body sizes, with intercastes being approximately 10% larger on average, and having some more queen-like traits (presence of vestigial eyes and four instead of two ovarioles) (9). This clonal raider ant study system has proven to be powerful in detecting phenotypic differences between clonal strains (5, 7) and is very well suited for teasing apart effects of genotype and environmental factors on caste allometry.

In PNAS, Piekarski et al. (9) tested the degree to which the allometric scaling relationships between body size and caste-related traits depend on genotype and rearing environment in the queenless clonal raider ant Ooceraea biroi.

In PNAS, Piekarski et al. (9) found that the three studied clonal genotypes showed differences in average body size and the likelihood to develop four ovarioles at a given body size. In contrast, while variation in three aspects of the larval rearing environment (food quantity, temperature, and caregiver genotype) affected body size and the likelihood to develop four ovarioles, the scaling relationship between body size and the likelihood to develop four ovarioles was insensitive to larval rearing environment (9).

The conditionality of caste allometry on genotype is very interesting but is not surprising. Variation between clonal lines for caste fate has previously been described in the clonal raider ant (7). The authors also previously identified “queen-like mutants” with vestigial eyes, four ovarioles, and wings in the clonal raider ant, and the scaling relationship between body size and these caste traits differed from wild type (5). Segregating genetic variants affecting caste allometry have also been found in other social insect populations (3, 4) and many of the queen-biasing genotypes that have been described may affect the relationship between body size and caste traits. Genetic variants affecting caste fate and caste allometry are expected to be maintained at low frequency by mutation–selection balance (16) if they are deleterious overall, but the high frequency of these variants in social insect populations seems to result from selection within and between colonies (5, 7, 8). Such genetic variation within and between populations offers exciting potential to map genetic factors affecting caste allometry.

A perhaps more surprising result of Piekarski et al. (9) is the robustness of the scaling relationship between body size and ovariole number to variation in the rearing environment. While the possibility of plasticity for allometry is often not considered, studies in a range of organisms have shown that allometric scaling between body size and other traits often does depend on environmental conditions such as temperature and nutrition quality (2). Is there something different about the clonal raider ant that may explain the observed insensitivity of caste allometry to variation in the rearing environment (9)? Perhaps the lack of queens releases the clonal raider ant from potential caste load (17) so that relatively canalized caste allometry might be favored by selection.

The experimental results from Piekarski et al. (9) beg further careful studies of caste allometry across other social insect species. For example, would similar results be found in Ooceraea species with a queen caste? Many ants have striking queen–worker dimorphism (Fig. 1). It seems reasonable to hypothesize that species with strong queen-worker dimorphism are more likely to have caste allometry that depends on multiple environmental factors (Fig. 1). In temperate species, queens are usually only reared in certain seasons while workers are reared across seasons (18). Ant queens also often have different protein and fat content than workers, so it seems likely that queen-destined ant larvae are fed qualitatively and quantitatively different diets (19), as is also the case in honey bees (3). It may be possible to achieve the same body size with different combinations of diet quantity and quality (or other environmental factors), which might result in different allometric scaling relationships between body size and other traits, as found in flies and other animals (2). Thus, environmental conditions such as temperature and nutrition quality might be expected to affect caste allometry in some social insect species (Fig. 1). The tight coupling of caste traits found in the clonal raider ant also differs from what has been found in other social insects such as the honey bee Apis mellifera, where in vitro rearing and in vivo grafting studies show that caste traits can be less integrated with each other and body size (3, 20). Both genotype and environmental conditions can lead to honey bees that are worker-sized with queen-like ovaries and have other unusual combinations of caste traits (4).

In PNAS, Piekarski et al. (9) have made excellent progress with the queenless clonal raider ant to test genetic and environmental effects on caste allometry. Further careful experimental manipulation of rearing environment conditions with a range of social insects will be necessary to evaluate the predictions of existing models. This experimental manipulation should explicitly target socially-regulated environmental factors, including socially-transferred molecules like juvenile hormone (21), which can cause changes in caste allometry, such as the development of ant workers that are queen-like in terms of size and morphology (22). The hourglass model may best fit species with weak queen–worker dimorphism (Fig. 1), which is the likely ancestral state of ants. It may also serve as a useful null hypothesis. The standard model may best fit species with strong queen–worker dimorphism (Fig. 1). Integrating components from both models, while also explicitly modeling the effects of social regulation (3, 23), may enable the development of a unified model that can help elucidate the expression and evolution of caste allometry across social insect lineages. A general model seems to have strong potential, given that intrinsic developmental genetic pathways affecting caste allometry seem to largely be shared between social insect lineages (24), involving highly conserved pathways underlying allometry and life history traits across animals (1, 18, 25).