Madeleine Beekman

Ancestral Monogamy Shows Kin Selection Is Key to the Evolution of Eusociality

Close relatedness has long been considered crucial to the evolution of eusociality. However, it has recently been suggested that close relatedness may be a consequence, rather than a cause, of eusociality. We tested this idea with a comparative analysis of female mating frequencies in 267 species of eusocial bees, wasps, and ants. We found that mating with a single male, which maximizes relatedness, is ancestral for all eight independent eusocial lineages that we investigated. Mating with multiple males is always derived. Furthermore, we found that high polyandry (>2 effective mates) occurs only in lineages whose workers have lost reproductive totipotency. These results provide the first evidence that monogamy was critical in the evolution of eusociality, strongly supporting the prediction of inclusive fitness theory.

Nature versus nurture in social insect caste differentiation

Recent evidence for genetic effects on royal and worker caste differentiation from diverse social insect taxa has put an end to the view that these phenotypes stem solely from a developmental switch controlled by environmental factors. Instead, the relative influences of genotypic and environmental effects on caste vary among species, ranging from largely environmentally controlled phenotypes to almost purely genetic systems. Disentangling the selective forces that generate variation for caste predisposition will require characterizing the genetic mechanisms underlying this variation, and identifying particular life-history strategies and kin structures associated with strong genetic effects on caste.

Phase transition between disordered and ordered foraging in Pharaoh's ants

The complex collective behavior seen in many insect societies strongly suggests that a minimum number of workers are required for these societies to function effectively. Here we investigated the transition between disordered and ordered foraging in the Pharaohs ant. We show that small colonies forage in a disorganized manner, with a transition to organized pheromone-based foraging in larger colonies. We also show that when food sources are difficult to locate through independent searching, this transition is first-order and exhibits hysteresis, comparable to a first-order phase transition found in many physical systems. To our knowledge, this is the first experimental evidence of a behavioral phase transition between a maladaptive (disorganized) and an adaptive (organized) state.

From nonlinearity to optimality: pheromone trail foraging by ants

Pheromone trails laid by foraging ants serve as a positive feedback mechanism for the sharing of information about food sources. This feedback is nonlinear, in that ants do not react in a proportionate manner to the amount of pheromone deposited. Instead, strong trails elicit disproportionately stronger responses than weak trails. Such nonlinearity has important implications for how a colony distributes its workforce, when confronted with a choice of food sources. We investigated how colonies of the Pharaohs ant, Monomorium pharaonis, distribute their workforce when offered a choice of two food sources of differing energetic value. By developing a nonlinear differential equation model of trail foraging, and comparing model with experiments, we examined how the ants allocate their workforce between the two food sources. In this allocation, the most profitable feeder (i.e. the feeder with the highest concentration of sugar syrup) was usually exploited by the majority of ants. The particular form of the nonlinear feedback in trail foraging means that when we offered the ants a choice between two feeders of equal profitability, foraging was biased to the feeder with the highest initial number of visitors. Taken together, our experiments illuminate how pheromones provide a mechanism whereby ants can efficiently allocate their workforce among the available food sources without centralized control.

Amoeboid organism solves complex nutritional challenges

A fundamental question in nutritional biology is how distributed systems maintain an optimal supply of multiple nutrients essential for life and reproduction. In the case of animals, the nutritional requirements of the cells within the body are coordinated by the brain in neural and chemical dialogue with sensory systems and peripheral organs. At the level of an insect society, the requirements for the entire colony are met by the foraging efforts of a minority of workers responding to cues emanating from the brood. Both examples involve components specialized to deal with nutrient supply and demand (brains and peripheral organs, foragers and brood). However, some of the most species-rich, largest, and ecologically significant heterotrophic organisms on earth, such as the vast mycelial networks of fungi, comprise distributed networks without specialized centers: How do these organisms coordinate the search for multiple nutrients? We address this question in the acellular slime mold Physarum polycephalum and show that this extraordinary organism can make complex nutritional decisions, despite lacking a coordination center and comprising only a single vast multinucleate cell. We show that a single slime mold is able to grow to contact patches of different nutrient quality in the precise proportions necessary to compose an optimal diet. That such organisms have the capacity to maintain the balance of carbon- and nitrogen-based nutrients by selective foraging has considerable implications not only for our understanding of nutrient balancing in distributed systems but for the functional ecology of soils, nutrient cycling, and carbon sequestration.

The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera

Honey bee workers maintain the brood nest of their colony within a narrow temperature range of 34.5±1.5°C, implying that there are significant fitness costs if brood is reared outside the normal range. However, the effects of abnormal incubation temperatures are subtle and not well documented. Here we show that short-term learning and memory abilities of adult workers are affected by the temperature they experienced during pupal development. In contrast, long-term learning and memory is not significantly affected by rearing temperature. Furthermore, we could detect no effects of incubation temperature on fluctuating asymmetry, as a measure of developmental stability, in workers, queens or drones. We conclude that the most important consequence of abnormal rearing temperatures are subtle neural deficiencies affecting short-term memory rather than physical abnormalities.

Reproductive conflicts in social animals: who has power?

Theoretical models are often used to analyze reproductive conflicts in animal societies; for example, by determining the different sex-allocation optima of queen and workers. But who is in control (queen or workers, dominant or subordinate) is normally an implicit or explicit assumption of the model. Here, we introduce the concept of power (the ability to do or act in a situation in which conflict over reproduction exists) and argue that the relative power of conflicting individuals or groups of individuals (e.g. the workers or subordinates) within a society can complement theoretical predictions to provide a deeper understanding of reproduction in animal societies. We also show that power involves both general principles, such as differences in the quality of the information available to conflicting parties, and idiosyncrasies of the biology of different taxa, such as viviparity versus oviparity. These idiosyncrasies can occur at any taxonomic level, from a single species to an entire order or class, and are often crucial for understanding the balance of power among conflicting parties.

Honeybee swarms : how do scouts guide a swarm of uninformed bees?

The organized movement of a swarm of honeybees towards its new home is a perplexing phenomenon because only a small number of scout bees, approximately 5%, know the direction in which the swarm has to move. Nevertheless, in the majority of cases a swarm, comprising about 10 000 mainly uninformed bees, reaches the new home. How do the scouts transfer directional information en route to the uninformed bees? We investigated a hypothesis proposed in the 1950s that suggests that scout bees fly rapidly through the airborne swarm, pointing towards the new home. We developed a model that simulates the movement of swarms and scouts and showed that when scouts fly through the swarm at a speed slightly higher than the speed of the other (uninformed) bees, they are indeed able to direct the swarm towards its new home. Hence, our model strongly supports the proposed hypothesis and shows that a collection of uninformed bees can be successfully guided by the purposeful movements of a small number of informed scouts.

Irrational decision-making in an amoeboid organism: transitivity and context-dependent preferences

Most models of animal foraging and consumer choice assume that individuals make choices based on the absolute value of items and are therefore ‘economically rational’. However, frequent violations of rationality by animals, including humans, suggest that animals use comparative valuation rules. Are comparative valuation strategies a consequence of the way brains process information, or are they an intrinsic feature of biological decision-making? Here, we examine the principles of rationality in an organism with radically different information-processing mechanisms: the brainless, unicellular, slime mould Physarum polycephalum. We offered P. polycephalum amoebas a choice between food options that varied in food quality and light exposure (P. polycephalum is photophobic). The use of an absolute valuation rule will lead to two properties: transitivity and independence of irrelevant alternatives (IIA). Transitivity is satisfied if preferences have a consistent, linear ordering, while IIA states that a decision makers preference for an item should not change if the choice set is expanded. A violation of either of these principles suggests the use of comparative rather than absolute valuation rules. Physarum polycephalum satisfied transitivity by having linear preference rankings. However, P. polycephalums preference for a focal alternative increased when a third, inferior quality option was added to the choice set, thus violating IIA and suggesting the use of a comparative valuation process. The discovery of comparative valuation rules in a unicellular organism suggests that comparative valuation rules are ubiquitous, if not universal, among biological decision makers.

Only full-sibling families evolved eusociality

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057–1062 (2010)10.1038/nature09205; Nowak et al. replyThe paper by Nowak et al. has the evolution of eusociality as its title, but it is mostly about something else. It argues against inclusive fitness theory and offers an alternative modelling approach that is claimed to be more fundamental and general, but which, we believe, has no practical biological meaning for the evolution of eusociality. Nowak et al. overlook the robust empirical observation that eusociality has only arisen in clades where mothers are associated with their full-sibling offspring; that is, in families where the average relatedness of offspring to siblings is as high as to their own offspring, independent of population structure or ploidy. We believe that this omission makes the paper largely irrelevant for understanding the evolution of eusociality.