Disruptive selection as a driver of evolutionary branching and caste evolution in social insects.

Theory suggests that evolutionary branching via disruptive selection may be a relatively common and powerful force driving phenotypic divergence. Here, we extend this theory to social insects, which have novel social axes of phenotypic diversification. Our model, built around turtle ant (Cephalotes) biology, is used to explore whether disruptive selection can drive the evolutionary branching of divergent colony phenotypes that include a novel soldier caste. Soldier evolution is a recurrent theme in social insect diversification that is exemplified in the turtle ants. We show that phenotypic mutants can gain competitive advantages that induce disruptive selection and subsequent branching. A soldier caste does not generally appear before branching, but can evolve from subsequent competition. The soldier caste then evolves in association with specialized resource preferences that maximize defensive performance. Overall, our model indicates that resource specialization may occur in the absence of morphological specialization, but that when morphological specialization evolves, it is always in association with resource specialization. This evolutionary coupling of ecological and morphological specialization is consistent with recent empirical evidence, but contrary to predictions of classical caste theory. Our model provides a new theoretical understanding of the ecology of caste evolution that explicitly considers the process of adaptive phenotypic divergence and diversification.

Seasonality in communication and collective decision-making in ants.

The ability of animals to adjust their behaviour according to seasonal changes in their ecology is crucial for their fitness. Eusocial insects display strong collective behavioural seasonality, yet the mechanisms underlying such changes are poorly understood. We show that nest preference by emigrating Temnothorax albipennis ant colonies is influenced by a season-specific modulatory pheromone that may help tune decision-making according to seasonal constraints. The modulatory pheromone triggers aversion towards low-quality nests and enhances colony cohesion in summer and autumn, but not after overwintering-in agreement with reports that field colonies split in spring and reunite in summer. Interestingly, we show that the pheromone acts by downgrading the perceived value of marked nests by informed and naive individuals. This contrasts with theories of collective intelligence, stating that accurate collective decision-making requires independent evaluation of options by individuals. The violation of independence highlighted here was accordingly shown to increase error rate during emigrations. However, this is counterbalanced by enhanced cohesion and the transmission of valuable information through the colony. Our results support recent claims that optimal decisions are not necessarily those that maximize accuracy. Other criteria-such as cohesion or reward rate-may be more relevant in animal decision-making.

Landscape genetics of a top neotropical predator.

Habitat loss and fragmentation as a consequence of human activities is a worldwide phenomenon and one of the major threats to global biodiversity. Habitat loss and fragmentation is particularly a concern in the biodiverse tropics, where deforestation is occurring at unprecedented rates. Although insects are one of the most diverse and functionally important groups in tropical ecosystems, the quantitative effect of landscape features on their gene flow remains unknown. Here, we used a robust landscape genetics approach to quantify the effect of ten landscape features (deforestation, mature forests, other forest types, the River Chagres, streams, stream banks, roads, sea, lakes and swamps) and interactions between them, on the gene flow of a neotropical forest keystone species, the army ant Eciton burchellii. The influence of landscape on E. burchellii's gene flow reflected the different dispersal capability of its sexes; aerial for males and pedestrian for females, and the different depths of population history inferred from microsatellites and mitochondrial DNA. In contrast to the gene flow-facilitating effect of mature forests, deforested areas were found to be strong barriers for E. burchellii's gene flow. Other forest types were found to be gene flow facilitators but only when interacting with mature secondary forests, therefore indicating the importance of mature forests for the survival of E. burchelii and its associate species. The River Chagres was identified as a major historical gene flow barrier for E. burchellii, suggesting that an important loss of connectivity may occur because of large artificial waterways such as the Panama Canal.

Group dynamics and record signals in the ant Temnothorax albipennis.

Many purely physical complex systems, in which there are both stochasticity and local interactions between the components, exhibit record dynamics. The temporal statistics of record dynamics is a Poisson process operating on a logarithmic rather than a linear time scale (i.e. a log-Poisson process). Record dynamics often drive substantial changes in complex systems when new high water marks in partially stochastic processes trigger new events. Social insect colonies are exemplary complex biological systems in which many of the local interactions of the components have been moulded by natural selection for the common good. Here, we combine experimental manipulation of ant colony demography with modelling to test the hypothesis that social interactions are the mechanism underlying the record dynamics. We found that compared with the control, log-Poisson statistics were disrupted in colonies in which the pattern of interactions was modified by the removal of the brood, and disappeared completely in 'callow' colonies composed entirely of very young workers from the same age cohort. We conclude that a subtle interplay between the demography of the society and the pattern of the interactions between the ants is crucial for the emergence of record dynamics. This could help identify what makes an ant colony a cohesive society.

Dispersal and population structure of a New World predator, the army ant Eciton burchellii.

The army ant Eciton burchellii is probably the most important arthropod predator in the Neotropics, and many animal species depend upon it. Sex-biased dispersal with winged males and permanently wingless queens may render this species especially sensitive to habitat fragmentation and natural barriers, which might have severe impacts on population structure and lead to population decline. Using nuclear microsatellite markers and mitochondrial sequences, we investigated genetic differentiation in a fragmented population in the Panama Canal area. While nuclear markers showed little differentiation between subpopulations (F(ST) = 0.017), mitochondrial differentiation was maximal in some cases (Phi(ST) = 1). This suggests that, while females are not capable of crossing barriers such as large rivers, flying males are able to promote nuclear gene flow between the studied forest patches. Consistent with this interpretation, we did not find any evidence for inbreeding or genetic deterioration on Barro Colorado Island over the last 90 years since its formation.

Why do house-hunting ants recruit in both directions?

To perform tasks, organisms often use multiple procedures. Explaining the breadth of such behavioural repertoires is not always straightforward. During house hunting, colonies of Temnothorax albipennis ants use a range of behaviours to organise their emigrations. In particular, the ants use tandem running to recruit naïve ants to potential nest sites. Initially, they use forward tandem runs (FTRs) in which one leader takes a single follower along the route from the old nest to the new one. Later, they use reverse tandem runs (RTRs) in the opposite direction. Tandem runs are used to teach active ants the route between the nests, so that they can be involved quickly in nest evaluation and subsequent recruitment. When a quorum of decision-makers at the new nest is reached, they switch to carrying nestmates. This is three times faster than tandem running. As a rule, having more FTRs early should thus mean faster emigrations, thereby reducing the colony's vulnerability. So why do ants use RTRs, which are both slow and late? It would seem quicker and simpler for the ants to use more FTRs (and higher quorums) to have enough knowledgeable ants to do all the carrying. In this study, we present the first testable theoretical explanation for the role of RTRs. We set out to find the theoretically fastest emigration strategy for a set of emigration conditions. We conclude that RTRs can have a positive effect on emigration speed if FTRs are limited. In these cases, low quorums together with lots of reverse tandem running give the fastest emigration.

Evolution of defence portfolios in exploiter-victim systems.

Some organisms maintain a battery of defensive strategies against their exploiters (predators, parasites or parasitoids), while others fail to employ a defence that seems obvious. In this paper, we shall investigate the circumstances under which defence strategies might be expected to evolve. Brood parasites and their hosts provide our main motivation, and we shall discuss why the reed warbler Acrocephalus scirpaceus has evolved an egg-rejection but not a chick-rejection strategy as a defence against the common (Eurasian) cuckoo Cuculus canorus, while the superb fairy-wren Malurus cyaneus has evolved a chick-rejection but not an egg-rejection strategy as a defence against Horsfield's bronze-cuckoo Chrysococcyx basalis. We suggest that the answers lie in strategy-blocking, where one strategy (the blocking strategy) prevents the appearance of another (the blocked strategy) that would be adaptive in its absence. This may be common in exploiter-victim systems.

Is dauer pheromone of Caenorhabditis elegans really a pheromone?

Animals respond to signals and cues in their environment. The difference between a signal (e.g. a pheromone) and a cue (e.g. a waste product) is that the information content of a signal is subject to natural selection, whereas that of a cue is not. The model free-living nematode Caenorhabditis elegans forms an alternative developmental morph (the dauer larva) in response to a so-called 'dauer pheromone', produced by all worms. We suggest that the production of 'dauer pheromone' has no fitness advantage for an individual worm and therefore we propose that 'dauer pheromone' is not a signal, but a cue. Thus, it should not be called a pheromone.

Self-organized lane formation and optimized traffic flow in army ants.

We show how the movement rules of individual ants on trails can lead to a collective choice of direction and the formation of distinct traffic lanes that minimize congestion. We develop and evaluate the results of a new model with a quantitative study of the behaviour of the army ant Eciton burchelli. Colonies of this species have up to 200 000 foragers and transport more than 3000 prey items per hour over raiding columns that exceed 100 m. It is an ideal species in which to test the predictions of our model because it forms pheromone trails that are densely populated with very swift ants. The model explores the influences of turning rates and local perception on traffic flow. The behaviour of real army ants is such that they occupy the specific region of parameter space in which lanes form and traffic flow is maximized.

Deciding on a new home: how do honeybees agree?

A swarm of honeybees (Apis mellifera) is capable of selecting one nest-site when faced with a choice of several. We adapt classical mathematical models of disease, information and competing beliefs to such decision-making processes. We show that the collective decision may be arrived at without the necessity for any bee to make any comparison between sites.

Arms races and the evolution of big fierce societies.

The causes of biological gigantism have received much attention, but only for individual organisms. What selection pressures might favour the evolution of gigantic societies? Here we consider the largest single-queen insect societies, those of the Old World army ant Dorylus, single colonies of which can have 20 million workers. We propose that colony gigantism in Dorylus arises as a result of an arms race and test this prediction by developing a size-structured mathematical model. We use this model for exploring and potentially explaining differences in colony size, colony aggression and colony propagation strategies in populations of New World army ants Eciton and Old World army ants Dorylus. The model shows that, by determining evolutionarily stable strategies (ESSs), differences in the trophic levels at which these army ants live feed forwards into differences in their densities and collision rates and, hence, into different strategies of growth, aggression and propagation. The model predicts large colony size and the occurrence of battles and a colony-propagation strategy involving highly asymmetrical divisions in Dorylus and that Eciton colonies should be smaller, non-combative and exhibit equitable binary fission. These ESSs are in excellent agreement with field observations and demonstrate that gargantuan societies can arise through arms races.

The possible role of reaction-diffusion in leaf shape.

We consider mechanisms that may determine certain simple leaf shapes. Compared with other aspects of plant morphogenesis, such as phyllotaxis or spiral leaf arrangement, rather little is known about leaf-shape-determining mechanisms. We develop mathematical models for the gross pattern of leaf shape based on reaction diffusion systems. These models are consistent with what is known about factors that might determine leaf shape. They show that diverse leaf shapes may be obtained from a single reaction diffusion system. This has implications in terms of both convergent and divergent evolution. The models make predictions that can be tested experimentally. We predict the form of pre-patterns of growth promoters in leaf primordia of different sizes when the morphogens either diffuse into the primordia or are produced locally. We also predict the effects on leaf shape of removing parts of primordia at different times. The models can also predict the effects on leaf shape of the topical application of activators and inhibitors to leaf primordia.

Ants estimate area using Buffon's needle.

We show for the first time, to our knowledge, that ants can measure the size of potential nest sites. Nest size assessment is by individual scouts. Such scouts always make more than one visit to a potential nest before initiating an emigration of their nest mates and they deploy individual-specific trails within the potential new nest on their first visit. We test three alternative hypotheses for the way in which scouts might measure nests. Experiments indicated that individual scouts use the intersection frequency between their own paths to assess nest areas. These results are consistent with ants using a 'Buffon's needle algorithm' to assess nest areas.

A model of survival times for predator populations: the case of the army ants.

We develop a method to estimate the expected time of survival of a predator population as a function of the size of the habitat island on which it lives and the dynamic parameters of the population and its prey. The model may be thought of either as a patch occupancy model for a structured population or as a model of metapopulation type. The method is applied to a keystone predator species, the neotropical army ant Eciton burchelli. Predictions are made as to how many of the islands and habitat islands in and around Gatun Lake in the Panama Canal, most of which were formed when the canal was dug, can be expected to support such a population today, and these are compared with data.

Doing the right thing: Ants, honeybees and naked mole-rats.

Traditionally the division of labour in social insects has been divided into two types: physical and temporal polyethism. New theoretical models indicate that temporal polyethism may be an emergent property rather than an organizational principle. Current research is revealing the relationship between temporal polyethism and the role of nonspecialized individuals within species of physically polymorphic social insects.

The organization of working teams' in social insects.

Preliminary optimization models for social insects suggested that efficiency should be promoted by having one specialist worker caste per essential task. However, such extreme specialization would greatly limit the ability of colonies to respond to changing situations and could lead to long periods of recession in a colony's economy. Recent studies show that by using simple behavioural rules social insects can reallocate tasks and form cooperative groups and even assembly lines that have far greater flexibility than would be the case with extremely specialized physical castes.

Evolutionary and ecological parallels between ants and fungi.

Despite their different fundamental organization, ant colonies and mycelia of fungi exhibit striking similarities in their social organization. Both are collectives of genetically related or identical semi-autonomous units, consisting respectively of discrete multicellular individuals and hyphae. There is a variety of parallels in their foraging and resource capture strategies, developmental versatility and division of labour, and in the interactions between non-self recognition phenomena resulting in sexual or parasitic invasion of foreign genes into the collective, or in rejection of non-self. These parallels lend a new perspective to the nutritional relationships and modes of communication between developmentally different phases in collective systems of interacting individual units. They also have important evolutionary implications for the origin and regulation of mechanisms of gene flow between different colonies or collectives, including a link between mechanisms underlying sex, parasitism and sympatric speciation.

Propaganda substances in the cuckoo antLeptothorax kutteri and the slave-makerHarpagoxenus sublaevis.

This paper reports the first discovery of "propaganda substances" in a workerless inquiline ant, the European myrmicineLeptothorax kutteri Buschinger. These substances are used by the parasite queen as a chemical weapon for defense against hostile workers of the host speciesL. acervorum. The substances also have an unusual behavioral effect: they cause host workers to attack each other, and they therefore appear to override nestmate recognition in host colonies. Laboratory experiments show that the source of these substances is the Dufour's gland of theL. kutteri queen. Our experiments also confirm the hypothesis that the closely related slave-making antHarpagoxenus sublaevis uses its Dufour's gland secretions as a chemical weapon during slave raids and colony foundation. The behavioral effect of these slave-maker secretions is identical to that ofL. kutteri queens.