Francis L. W. Ratnieks

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.

Conflict in single-queen hymenopteran societies: the structure of conflict and processes that reduce conflict in advanced eusocial species

Social insect workers can increase their inclusive fitness by increasing colony production of reproductives, by manipulating the identity of colony reproductives in favor of individuals with greater kin-value (e.g. relatedness) to themselves, or both. The manipulative option results from the non-clonal genetic structure of insect societies and necessarily introduces conflict into insect societies. This paper examines conflict over male production, queen-rearing, and sex allocation for monogynous hymenopteran societies. The structure of conflict is shown to vary according to the particular conflict, queen mating frequency, and other factors. Importantly, there are conditions under which the actual conflict (i.e. the actual manipulation of reproduction) is predicted to be markedly less than the potential conflict (i.e. all the manipulations potentially beneficial to individual workers given the kin-value asymmetries within the colony). For example, when manipulation is costly (i.e. reduces colony productivity), or relatively ineffective (i.e. because of limitations to kin recognition ability, or counter manipulations such as worker policing) it may be selectively disfavored. Furthermore, low actual conflict may be characteristic of certain sub-sets of workers (e.g. foragers) or certain phases of colony growth (e.g. the ergonomic phase). As a result, a pluralistic rather than a typological perspective on conflict in insect societies is suggested. Low actual conflict may facilitate the evolution of colony- or group-level adaptations (i.e. attributes of individuals which have evolved to enable them to function synergistically as a colony or group, such as social foraging in honey bees and army ants), despite the non-clonal genetic structure of most insect societies. However, low levels of actual conflict between individuals need not result in group-level adaptations. The term community of interest is suggested to describe groups within which there is little or no actual conflict, whether or not group-level adaptations occur. The recently revived term superorganism is problematic, because it is often used in a categorical way, to describe whole societies. This difficulty is partly overcome by the pluralistic outlook, which would favor statements such as “foraging in the honey bee shows superorganismic properties” (i.e. group-level adaptations), rather than typological thinking such as “the honey bee colony is a superorganism”.

Task partitioning in insect societies

Summary: Task partitioning is the name given to the phenomenon in which a piece of work is divided among two or more workers, such as the partitioning of the collection of a load of forage between a forager and a storer or transporter. This study 1) reviews empirical data concerning the occurrence of task partitioning in insect societies with the general aim of drawing broad conclusions about its prevalence and diversity, and 2) considers the potential costs and benefits of task partitioning. The data show that task partitioning occurs in many species, with examples in ants, bees, wasps, and termites. The general impression is that it is an important and widespread feature of work organisation in insect societies. Nearly all examples concern foraging. There is much variation on the main theme. For example, in the number of intersecting cycles (2, 3 linear, 3 all interlocking), where transfer occurs (at the nest, at the forage site, on the trail back to the nest), whether transfer is direct or indirect (liquids such as nectar, water, and honeydew are always transferred directly whereas solids are transferred both directly and indirectly). Task partitioning is always subject to time costs. Benefits occur either through enhancement of individual performance (e.g., where task partitioning permits greater division of labour thereby utilising consistent differences in worker abilities caused by morphology or experience) or through enhancement of the overall system (e.g., where partitioning itself eliminates a constraint affecting task performance, such as when a forager can collect sufficient material for several builders). By causing a series organisation of work, task partitioning reduces system reliability but this effect may be minimal in all but very small colonies.

Clarity on Honey Bee Collapse

The worldwide losses of honey bee colonies continue to puzzle researchers and the beekeeping industry. Over the past few years, the media have frequently reported deaths of honey bee (Apis mellifera L.) colonies in the United States, Europe, and Japan. Most reports express opinions but little hard science. A recent historical survey (1) pointed out that extensive colony losses are not unusual and have occurred repeatedly over many centuries and locations. Concern for honey bees in the United States has been magnified by their vital role in agriculture. The California almond industry alone is worth

Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory

2 billion annually and relies on over 1 million honey bee hives for cross-pollination. So what is killing honey bee colonies worldwide, and what are the implications for agriculture?

Egg-laying, egg-removal, and ovary development by workers in queenright honey bee colonies

In many bees, wasps, and ants, workers police each other in order to prevent individual workers from selfishly producing their own male offspring. Although several factors can selectively favor worker policing, genetic relatedness is considered to be of special importance. In particular, kin selection theory predicts that worker policing should be more common in species where workers are more related to the queen’s sons than to other workers’ sons. Here we provide strong novel support for this theory based on a comparative analysis of policing and male parentage in 109 species of ants, bees, and wasps. First, an analysis of behavioral data confirms that worker policing occurs more frequently in species where workers are more related to the queen’s sons than to other workers’ sons. Second, an analysis of male parentage shows that a significantly higher percentage of the males are workers’ sons in species where the workers are more related to other workers’ sons. Both conclusions also hold if data are analyzed using phylogenetically independent contrasts. Although our analysis provides strong overall support for the theory that relatedness affects kin conflict over male parentage, there is also significant residual variation. Several factors that may explain this variation are discussed.

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

SummaryThe study investigates whether worker policing via the selective removal of worker-laid male eggs occurs in normal honey bee colonies with a queen. Queenright honey bee colonies were set up with the queen below a queen excluder. Frames of worker brood and drone comb were placed above the queen excluder. Daily inspections of the drone frames revealed the presence of a few eggs, presumably laid by workers, at a rate of 1 egg per 16000 drone cells. 85% of these eggs were removed within 1 day and only 2% hatched. Dissections of workers revealed that about 1 worker in 10000 had a fully developed egg in her body. These data show that worker egg-laying and worker policing are both normal, though rare, in queenright honey bee colonies, and provide further confirmation of the worker policing hypothesis.

Worker reproduction and policing in insect societies: an ESS analysis

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.

Enforced altruism in insect societies

Insect societies are vulnerable to exploitation by workers who reproduce selfishly rather than help to rear the queens offspring. In most species, however, only a small proportion of the workers reproduce. Here, we develop an evolutionarily stable strategy (ESS) model to investigate factors that could explain these observed low levels of reproductive exploitation. Two key factors are identified: relatedness and policing. Relatedness affects the ESS proportion of reproductive workers because laying workers generally work less, leading to greater inclusive fitness costs when within‐colony relatedness is higher. The second key factor is policing. In many species, worker‐laid eggs are selectively removed or ‘policed’ by other workers or the queen. We show that policing not only prevents the rearing of worker‐laid eggs but can also make it unprofitable for workers to lay eggs in the first place. This can explain why almost no workers reproduce in species with efficient policing, such as honeybees, Apis, and the common wasp, Vespula vulgaris, despite relatively low relatedness caused by multiple mating of the mother queen. Although our analyses focus on social insects, the conclusion that both relatedness and policing can reduce the incentive for cheating applies to other biological systems as well.

Trail geometry gives polarity to ant foraging networks

Cooperation among workers and their seeming altruism result from strict policing by nestmates.