Ruling the unruly: Innovation in ant larval feeding led to increased caste dimorphism and social complexity

Abstract

Differences between reproductive and worker castes are essential to eusocial societies. The morphological chasm between castes is highly heterogeneous across the ant phylogeny. The low size dimorphism of basal ant lineages suggests that evolutionary innovations occurred during the diversification of ants, potentially enabling their major evolutionary transition from simple eusocial societies to superorganisms. We measured queen and worker body volumes of 321 ant species belonging to 124 genera and 13 subfamilies to investigate the correlation between dimorphism and a panel of traits linked to complex eusociality. Using comparative phylogenetic methods, we show that higher dimorphism is associated with large colony sizes, distinct worker subcastes, and the loss of worker ability to mate. However, these traits correlate with both dimorphism and body volume variations of female castes. In contrast, larval morphology associated with passive larval behavior correlates only with dimorphism and not body volume variations of queens and workers. We argue that creating a large size differential between totipotent larvae with identical reproductive aspirations requires firm colony control over larval caste fate, which can only be exerted if larval nutrition is regulated by workers. We suggest that the evolutionary innovation of individualized worker-to-larva feeding, for example through trophallaxis, brought about passive larvae in some major ant lineages. Our results indicate that resolution of the conflict between larval reproductive aspirations and colony priorities was a necessary step in the evolution of complex eusocial societies.

Coevolution of larval signalling and worker response can trigger developmental caste determination in social insects

“…Therefore, larval signalling strategies that lead to worker polymorphism might not evolve in such a scenario. However, conflicts about future reproductive abilities by larvae could also be resolved by firm worker control of larval nutrition, as suggested by a recent comparative analysis on the evolution of queen–worker dimorphism [70] and by models on caste fate conflict [71]. Another mechanism for overcoming selfish larval signalling strategies is worker policing.…”

Social administration of juvenile hormone to larvae increases body size and nutritional needs for pupation

“…Potentially this enzyme might represent an adaptation to ensure worker behavioural integrity, despite the high titre of juvenile hormone that must be produced to be fed to larvae. Finally, a developmental dependency of larvae on workers could be a colony-level mechanism for ensuring a social control of larval development and reducing conflict between larvae and the rest of the colony regarding their developmental trajectory [ 53 ].…”

Metabolic division of labor in social insects

“…In contrast to nectar and pollen, the royal jelly synthesized by honeybee nurses is a highly elaborated cocktail of proteins and macromolecules [49,50]. Thus, metabolic division of labor may be an adaptive mechanism to manipulate larval diet quality and thus build adaptive asymmetries within the collective (e.g body size, longevity; Figure 2, [51]).…”

“…Metabolic division of labor can minimize metabolic costs for reproductives, relegate those costs to more disposable workers or larvae and thus maximize the lifespan and egg production of the reproductive(s), beneficial to colony fitness (Figure 2, [51]). For instance the process of digestion is metabolically costly but essential for nutrient intake.…”

“…These asymmetries can have developmental and life history consequences [51][52][53] including the adult size dimorphism or differences in longevity and fecundity between reproductives and workers (Figure 2). Termites workers are lacking of uric-acid oxidase which prevent them from using stocks of uric acid as a source of nitrogen; instead this enzyme is highly abundant in reproductives which can thus metabolize uric acid that they receive from non-reproductives and use this nitrogen source for their reproduction [20].…”