Diana E. Wheeler

Developmental and Physiological Determinants of Caste in Social Hymenoptera: Evolutionary Implications

Ants, bees, and wasps form societies made up almost entirely of females. The societies are structured by differences among female members; these may be subtle, involving only physiology, or profound, involving gross size differences and hundreds of morphological characters. Since adult morphology is the product of development, the developmental systems that generate different female forms must be fundamental to social structure. Increased complexity of social organization requires changes in the underlying developmental programs that produce the members of a society. In this paper, I present a developmental view of the evolution of societies. These insights serve as a bridge between theories focused on the initial stages of the evolution of sociality in Hymenoptera (Hamilton 1964; Lin and Michener 1972; West-Eberhard 1975) and theories focused on the evolution of insect societies as superorganisms (Oster and Wilson 1978). In simple social systems, the struggle for control of the reproductive physiology of nest mates is resolved entirely in the adult stage; all females are potential queens. The evolution of higher sociality involves an enhancement of the differences between nonreproductive workers and reproductive queens. In what are termed primitively eusocial species, queens and workers cannot be distinguished on the basis of external structure. Size differences, however, often do exist. By contrast, queens and workers differ morphologically in the highly eusocial species (Michener 1974). (A eusocial society must, by definition, have both reproductive division of labor [reproductive castes] and overlap between generations, so that offspring assist parents in brood care [Wilson 1971].) The evolutionary divergence of queen and worker morphology raises two complementary questions regarding the relationship between social structure and the factors that determine physical or physiological differences among females. How far can the physiological and morphological gap between workers and queens be widened in simple systems

The developmental basis of worker caste polymorphism in ants

Among social Hymenoptera, the evolution of the worker caste has reached its apex in the ants, in which some taxa have evolved complex physical worker caste systems. Diverse worker caste systems can be generated through regulation of three aspects of larval growth: critical size, growth parameters, and reprogramming of these factors. Even the most complex caste systems could have evolved simply by the addition of revised programs to the end of an ancestral developmental pathway for workers. Worker castes in ants provide a system in which to study the evolution of reaction norms and developmental switches. In ants, the simplest developmental switch, revision of critical size alone, does not lead to discontinuous phenotypes. Only when changes in growth rules are tied to the decision to revise critical size are distinct phenotypes produced from the alternative developmental programs. The addition of ever more physical castes may be limited by both developmental and ecological factors.

Expression of insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera.

Female honeybees have two castes, queens and workers. Developmental fate is determined by larval diet. Coding sequences made available through the Honey Bee Genome Sequencing Consortium allow for a pathway‐based approach to understanding caste determination. We examined the expression of several genes of the insulin signalling pathway, which is central to regulation of growth based on nutrition. We found one insulin‐like peptide expressed at very high levels in queen but not worker larvae. Also, the gene for an insulin receptor was expressed at higher levels in queen larvae during the 2nd larval instar. These results demonstrate that the insulin pathway is a compelling candidate for pursing the relationship between diet and downstream signals involved in caste determination and differentiation.

Expression profiles during honeybee caste determination

BackgroundDepending on their larval environment, female honeybees develop into either queens or workers. As in other polyphenisms, this developmental switch depends not on genomic differences between queens and workers but on the differential expression of entire suites of genes involved with larval fate. As such, this and other polyphenic systems can provide a novel tool for understanding how genomes and environmental conditions interact to produce different developmental trajectories. Here we use gene-expression profiles during honeybee caste determination to present the first genomic view of polyphenic development.ResultsLarvae raised as queens or workers differed greatly in their gene-expression patterns. Workers remained more faithful than queens to the expression profiles of younger, bipotential, larvae. Queens appeared to both downregulate many of the genes expressed by bipotential larvae and turn on a distinct set of caste-related genes. Queens overexpressed several metabolic enzymes, workers showed increased expression of a member of the cytochrome P450 family, hexameric storage proteins and dihydrodiol dehydrogenase, and young larvae overexpressed two putative heat-shock proteins (70 and 90 kDa), and several proteins related to RNA processing and translation.ConclusionsLarge differences in gene expression between queens and workers indicate that social insect castes have faced strong directional selection pressures. Overexpression of metabolic enzymes by queen-destined larvae appears to reflect the enhanced growth rate of queens during late larval development. Many of the differently expressed genes we identified have been tied to metabolic rates and cellular responses to hormones, a result consistent with known physiological differences between queen and worker larvae.

Gene expression and the evolution of insect polyphenisms

Polyphenic differences between individuals arise not through differences at the genome level but as a result of specific cues received during development. Polyphenisms often involve entire suites of characters, as shown dramatically by the polyphenic castes found in many social insect colonies. An understanding of the genetic architecture behind polyphenisms provides a novel means of studying the interplay between genomes, gene expression and phenotypes. Here we discuss polyphenisms and molecular genetic tools now available to unravel their developmental bases in insects. We focus on several recent studies that have tracked gene‐expression patterns during social insect caste determination. BioEssays 23:62–68, 2001. Published 2001 John Wiley & Sons, Inc.

GROWTH MODELS OF COMPLEX ALLOMETRIES IN HOLOMETABOLOUS INSECTS

Allometries among body parts of adult holometabolous insects differ from allometries among body parts of many other animals because adult structures (many of which are derived from imaginal disks) do not grow synchronously with the body. Imaginal structures grow little during larval life but experience most of their growth during the prepupal and pupal period, after food intake and somatic growth have ceased. Growth of imaginal tissues thus occurs in a closed system at the expense of nutrients accumulated during larval life. In a closed system, growing imaginal tissues compete for available nutrients, and the growth trajectory and final size of one tissue (or disk) are influenced by the growth of others. We use the Gompertz growth equation and a model of growth in a closed system in which imaginal disks compete for nutrients to model the growth of imaginal disks and the resulting allometric relations among them. By incorporating known features of ant caste development, such as reprogramming of the critical size for metamorphosis in major workers (soldiers) and reprogramming of developmental parameters in individuals larger than a critical size, we show that the nonlinear and discontinuous allometries of ants with polymorphic castes result from normal developmental processes during the metamorphosis of holometabolous insects. The imaginal disk competition model predicts that when one disk is reprogrammed, others will show a compensatory response. Such correlated developmental responses may play a role in the evolution of body proportions in ants, rhinoceros beetles, and other insects.

Ancestral Developmental Potential Facilitates Parallel Evolution in Ants

Supersoldier Throwbacks Anomalous traits reflecting those of an ancestor sporadically appear in individuals that normally should not have them. Through their work with the hyperdiverse ant genus Pheidole, Rajakumar et al. (p. 79) suggest that these anomalies represent raw materials for selection to act upon. The ants possess an ancestral developmental potential, to produce “supersoldiers,” that has been retained for over 30 million years for which recurrent induction has facilitated the adaptive and parallel evolution of supersoldiers. The potential for developing “supersoldiers” has remained dormant in the ant genus Pheidole for at least 30 million years. Complex worker caste systems have contributed to the evolutionary success of advanced ant societies; however, little is known about the developmental processes underlying their origin and evolution. We combined hormonal manipulation, gene expression, and phylogenetic analyses with field observations to understand how novel worker subcastes evolve. We uncovered an ancestral developmental potential to produce a “supersoldier” subcaste that has been actualized at least two times independently in the hyperdiverse ant genus Pheidole. This potential has been retained and can be environmentally induced throughout the genus. Therefore, the retention and induction of this potential have facilitated the parallel evolution of supersoldiers through a process known as genetic accommodation. The recurrent induction of ancestral developmental potential may facilitate the adaptive and parallel evolution of phenotypes.

Endocrine Influences on the Organization of Insect Societies

We review evidence for endocrine influences on division of labor in insect societies. Juvenile hormone (JH) has been studied most extensively. JH is involved in control of four forms of division of labor: division of labor for reproduction among adults, division of labor for reproduction via caste differentiation, division of labor for colony growth and development among adults, and division of labor for colony growth and development via physical castes. Ecdysteroids, biogenic amines, and insulin have begun to be studied in these contexts as well. Ecdysteroids are implicated in the control of caste determination and reproductive maturation in bees. Octopamine influences the division of labor among workers, octopamine and serotonin exert neurohormonal influences on the production of JH by the corpora allata, and octopamine and dopamine levels are correlated suggestively with aspects of reproductive development in bumblebees, honeybees, and paper wasps. Insulin signaling is involved in caste determination and division of labor among workers. Vitellogenin, best known as a yolk protein, may also have hormone-like functions in the regulation of division of labor among workers. We present a verbal model that proposes that evolutionary changes in endocrine function play key roles in the evolution of division of labor.

Highly similar microbial communities are shared among related and trophically similar ant species.

Ants dominate many terrestrial ecosystems, yet we know little about their nutritional physiology and ecology. While traditionally viewed as predators and scavengers, recent isotopic studies revealed that many dominant ant species are functional herbivores. As with other insects with nitrogen‐poor diets, it is hypothesized that these ants rely on symbiotic bacteria for nutritional supplementation. In this study, we used cloning and 16S sequencing to further characterize the bacterial flora of several herbivorous ants, while also examining the beta diversity of bacterial communities within and between ant species from different trophic levels. Through estimating phylogenetic overlap between these communities, we tested the hypothesis that ecologically or phylogenetically similar groups of ants harbor similar microbial flora. Our findings reveal: (i) clear differences in bacterial communities harbored by predatory and herbivorous ants; (ii) notable similarities among communities from distantly related herbivorous ants and (iii) similar communities shared by different predatory army ant species. Focusing on one herbivorous ant tribe, the Cephalotini, we detected five major bacterial taxa that likely represent the core microbiota. Metabolic functions of bacterial relatives suggest that these microbes may play roles in fixing, recycling, or upgrading nitrogen. Overall, our findings reveal that similar microbial communities are harbored by ants from similar trophic niches and, to a greater extent, by related ants from the same colonies, species, genera, and tribes. These trends hint at coevolved histories between ants and microbes, suggesting new possibilities for roles of bacteria in the evolution of both herbivores and carnivores from the ant family Formicidae.

Soldier determination in Pheidole bicarinata: Inhibition by adult soldiers

Abstract In the ant Pheidole bicarinata, adult soldiers suppress the induction of soldier developments in larvae that have been treated with methoprene, as well as in acetone-treated controls. Induction of soldier development is inhibited in methoprene-treated larvae when the adult soldiers are present as nurses, when they are present in the colony but minor workers serve as nurses, and when they are held in a minor worker-permeable cage to prevent them from contacting larvae. Suppression of soldier determination can be overridden by high doses of methoprene applied during the juvenile hormone-sensitive period for soldier determination. The degree of suppression increases with increasing contact between larvae and adult soldiers. The most likely mechanism of inhibition is a contact soldier pheromone. On the basis of our results, we expand our model of soldier determination to accommodate the fact that the threshold titre of juvenile hormone necessary to induce soldier development changes in the presence of soldiers. A threshold that is sensitive to the presence of adult soldiers provides a mechanism whereby the worker caste ratio in colonies can be regulated.