Rebecca M. Clark

Division of labour and socially induced changes in response thresholds in associations of solitary halictine bees

Division of labour is a recurrent property of social groups. Among the different models proposed to explain the origin of division of labour, response-threshold models have garnered strong theoretical and empirical support. These models postulate that task specialization can arise spontaneously from interindividual variation in thresholds for responding to task-associated stimuli. Consequently, individuals with lower thresholds for a given task are more likely to become specialists. Self-reinforcement models expand this hypothesis by proposing that the successful performance of a task lowers an individuals threshold, increasing the probability that it will perform that task again. Although an important component of many models of division of labour, self-reinforcement can be difficult to test in real-world contexts. Here, we asked whether social experience modulates the individual response thresholds of normally solitary individuals. We focused on task performance during the early stages of nest construction in forced associations of the normally solitary halictine bee Lasioglossum (Ctenonomia) NDA-1. Within each pair, a strong behavioural asymmetry arose, with one bee specializing in excavation and her nestmate specializing in guarding the nest entrance. Individual performance of excavation by each bee was compared before and after being paired with a conspecific. After experiencing a social environment, individuals substantially increased their excavation performance. However, bees excavating more frequently in groups did not excavate differentially more afterwards, as would be predicted by self-reinforcement. The social context experienced by bees seems to promote behavioural differentiation leading to task specialization and to modulate response thresholds for excavation.

Nutritional physiology of life history trade-offs: how food protein-carbohydrate content influences life-history traits in the wing-polymorphic cricket Gryllus firmus

Although life-history trade-offs result from the differential acquisition and allocation of nutritional resources to competing physiological functions, many aspects of this topic remain poorly understood. Wing-polymorphic insects, which possess alternative morphs that trade off allocation to flight capability versus early reproduction, provide a good model system for exploring this topic. In this study, we used the wing-polymorphic cricket Gryllus firmus to test how expression of the flight capability versus reproduction trade-off was modified across a heterogeneous protein–carbohydrate nutritional landscape. Newly molted adult female long- and short-winged crickets were given one of 13 diets with different concentrations and ratios of protein and digestible carbohydrate; for each cricket, we measured consumption patterns, growth and allocation to reproduction (ovary mass) versus flight muscle maintenance (flight muscle mass and somatic lipid stores). Feeding responses in both morphs were influenced more by total macronutrient concentration than by protein–carbohydrate ratio, except at high-macronutrient concentration, where protein–carbohydrate balance was important. Mass gain tended to be greatest on protein-biased diets for both morphs, but was consistently lower across all diets for long-winged females. When long-winged females were fed high-carbohydrate foods, they accumulated greater somatic lipid stores; on high-protein foods, they accumulated greater somatic protein stores. Food protein–carbohydrate content also affected short-winged females (selected for early reproductive onset), which showed dramatic increases in ovary size, including ovarian stores of lipid and protein, on protein-biased foods. This is the first study to show how the concentration and ratio of dietary protein and carbohydrate affects consumption and allocation to key physiological features associated with the reproduction–dispersal life-history trade-off.

BEHAVIORAL REGULATION OF GENETIC CASTE DETERMINATION IN A POGONOMYRMEX POPULATION WITH DEPENDENT LINEAGES

The fate of a social insect colony is partially determined by its ability to allocate individuals to the caste most appropriate for the requirements for growth, maintenance, and reproduction. In pairs of dependent lineages of Pogonomyrmex barbatus, the allocation of individuals to the queen or worker caste is constrained by genotype, a system known as genetic caste determination (GCD). In mature GCD colonies, interlineage female eggs develop into sterile workers, while intralineage eggs become reproductively capable queens. Although the population-level consequences of this system have been intensively studied, the proximate mechanisms for GCD remain unknown. To elucidate these mechanisms, we brought newly mated queens into the laboratory and allowed them to establish colonies, nearly half of which unexpectedly produced virgin queens only seven months after colony founding. We genotyped eggs, workers, and the virgin queens from these colonies. Our results showed that queens in young colonies produce both interlineage and intralineage eggs, demonstrating that queens of GCD colonies indiscriminately use sperm of at least two lineages to fertilize their eggs. Intralineage eggs were more frequent in colonies producing virgin queens. These findings suggest that intralineage eggs are predetermined to become queens and that workers may cull these eggs when colonies are not producing queens. Virgin queens produced by young GCD colonies were smaller than field-caught virgin queens, and often had developmental problems. Hence, they are probably nonfunctional and represent an intense resource drain for developing colonies, not a contribution to colony fitness.

Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens

Research on the evolution of cooperative groups tends to explore the costs and benefits of cooperation, with less focus on the proximate behavioral changes necessary for the transition from solitary to cooperative living. However, understanding what proximate changes must occur, as well as those pre-conditions already in place, is critical to understanding the origins and evolution of sociality. The California harvester ant Pogonomyrmex californicus demonstrates population-level variation in colony founding over a close geographic range. In adjacent populations, queens either found nests as single individuals (haplometrosis) or form cooperative groups of nonrelatives (pleometrosis). We compared aggregation, aggression, and tolerance of queens from one pleometrotic and two haplometrotic populations during nest initiation, to determine which behaviors show an evolutionary shift and which are present at the transition to pleometrosis. Surprisingly, within-nest aggregative behavior was equally present among all populations. In nesting boxes with multiple available brood-rearing sites, both queen types readily formed and clustered around a single common brood pile, suggesting that innate attraction to brood (offspring) facilitates the transition to social aggregation. In contrast, queens from the three populations differed in their probabilities of attraction on the ground to nest sites occupied by other queens and in levels of aggression. Our results suggest that some key behavioral mechanisms facilitating cooperation in P. californicus are in place prior to the evolution of pleometrosis and that the switch from aggression to tolerance is critical for the evolution of stable cooperative associations.

Nutrient regulation strategies differ between cricket morphs that trade‐off dispersal and reproduction

Summary 1. Nutrient regulation should covary with life history, but actual demonstrations of this connection are rare. 2. Here, we use a wing-polymorphic cricket, Gryllus firmus, that trades off dispersal and reproduction; the long-winged morph with functional flight muscles [LW(f)] is adapted for dispersal at the expense of egg production, while the short-winged (SW) morph is adapted for egg production at the expense of flight. We explore the extent to which these two morphs differentially regulate macronutrient intake to best match their life-history strategy. 3. In a ‘choice’ experiment, we offered female crickets of each morph [LW(f) and SW] two nutritionally complementary foods varying in protein and digestible carbohydrate content. In a second ‘no-choice’ experiment, we confined crickets to one of five foods, each with a different protein/carbohydrate ratio. In both experiments, and for both morphs, we measured food intake, mass gain and lipid concentration. 4. In the ‘choice’ experiments, LW(f) females selected a more carbohydrate-biased diet than SW females. The two morphs gained similar total mass, but the LW morph had higher lipid concentration. 5. In the no-choice experiment, the two morphs practised different nutrient ‘consumption rules’. SW females ate similar total nutrient amounts (protein plus carbohydrate) across diets, while LW(f) females decreased intake as the protein/carbohydrate ratio of the available food became increasingly imbalanced. Overall mass gain was marginally higher in the SW morph and lowest for both morphs on the diets that were extremely carbohydrate biased. LW(f) and SW females had similar lipid concentrations across the diets, even though LW(f) crickets ate less carbohydrate on the two carbohydrate-biased diets. Our data suggest that for LW(f) females, there are costs of overeating nutrients in excess of requirements, but they are efficient at utilizing ingested nutrients. 6. Our results shed new light on how the nutritional environment interacts with the direct trade-off between dispersal and reproduction occurring in adult G. firmus crickets. Dispersal is linked to heightened diet selectivity and an emphasis on nutrients promoting flight fuel (lipid) storage over protein acquisition for egg laying, such that nutritional regulation complements the metabolic mechanisms that generate this trade-off.

Social insects inspire human design

The international conference ‘Social Biomimicry: Insect Societies and Human Design’, hosted by Arizona State University, USA, 18–20 February 2010, explored how the collective behaviour and nest architecture of social insects can inspire innovative and effective solutions to human design challenges. It brought together biologists, designers, engineers, computer scientists, architects and businesspeople, with the dual aims of enriching biology and advancing biomimetic design.

Lipogenesis in a wing-polymorphic cricket: Canalization versus morph-specific plasticity as a function of nutritional heterogeneity

The influence of variable nutritional input on life history adaptation is a central, but incompletely understood aspect of life history physiology. The wing-polymorphic cricket, Gryllus firmus, has been extensively studied with respect to the biochemical basis of life history adaptation, in particular, modification of lipid metabolism that underlies the enhanced accumulation of lipid flight fuel in the dispersing morph [LW(f)=long wings with functional flight muscles] relative to the flightless (SW=short-winged) morph. To date, biochemical studies have been undertaken almost exclusively using a single laboratory diet. Thus, the extent to which nutritional heterogeneity, likely experienced in the field, influences this key morph adaptation is unknown. We used the experimental approach of the Geometric Framework for Nutrition and employed 13 diets that differed in the amounts and ratios of protein and carbohydrate to assess how nutrient amount and balance affects morph-specific lipid biosynthesis. Greater lipid biosynthesis and allocation to the soma in the LW(f) compared with the SW morph (1) occurred across the entire protein-carbohydrate landscape and (2) is likely an important contributor to elevated somatic lipid in the LW(f) morph across the entire protein-carbohydrate landscape. Nevertheless, dietary carbohydrate strongly affected lipid biosynthesis in a morph-specific manner (to a greater degree in the LW(f) morph). Lipogenesis in the SW morph may be constrained due to its more limited lipid storage capacity compared to the LW(f) morph. Elevated activity of NADP+-isocitrate dehydrogenase (NADP+-IDH), an enzyme that produces reducing equivalents for lipid biosynthesis, was correlated with and may be an important cause of the increased lipogenesis in the LW(f) morph across most, but not all regions of the protein-carbohydrate landscape. By contrast, ATP-citrate lyase (ACL), an enzyme that catalyzes the first step in the pathway of fatty acid biosynthesis, showed complex morph-specific patterns of activity that were strongly contingent upon diet. Morph-specific patterns of NADP+-IDH and ACL activities across the nutrient landscape were much more complex than expected from previous studies on a single diet. Collectively, our results indicate that the biochemical basis of an important life history adaptation, morph-specific lipogenesis, can be canalized in the face of substantial nutritional heterogeneity. However, in some regions of the protein-carbohydrate landscape, it is strongly modulated in a morph-specific manner.