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.     

How much do army ants eat? On the prey intake of a neotropical top-predator

New World army ants (Ecitoninae) are nomadic group-predators that are widely thought to have a substantial impact on their prey. Nevertheless, quantitative data on prey intake by army ants is scarce and mostly limited to chance encounters. Here, I quantify the prey intake of the army ant Eciton hamatum at the contrasting scales of raid, colony (sum of simultaneous raids), and population. Like most army ants, E. hamatum conducts narrow ‘column raids’ and has a specialized diet of ant prey. I show that individual raids often had periods of no prey intake, and raid intake rates, calculated in g/min, differed significantly among colonies. Moreover, neither mean nor peak raid intake rates were correlated with colony size. Similarly, colony intake rates differed significantly among colonies, and mean colony intake rates were not correlated with colony size. However, mean colony intake rates were significantly higher than mean raid intake rates, and peak colony intake rate was correlated with colony size. Having multiple raids thus improves colony-level intake rates, and larger colonies can harvest more prey per unit time. Mean colony intake rate across colonies was 0.067 g/min dry weight and mean daily colony intake was calculated at 38.2 g. This intake is comparable to that of Eciton burchellii, which has a more generalized diet and conducts spectacular ‘swarm raids’ that are seen as having a greater impact on prey than column raids. Population size on Barro Colorado Island, Panama, was estimated to be 57 colonies, which extrapolates to a daily population intake of nearly 2 kg of prey dry weight, or 120 g/km². Broadly, these findings demonstrate that column raiding army ants experience considerable variation in prey intake for individual raids, but can still achieve notable impact at the larger scales of colony and population. Furthermore, they challenge the idea that swarm-raiding species necessarily have greater intake and thus impact on prey. Instead, I suggest that conducting multiple column raids may be a strategy that allows for comparable intake from a more specialized diet.     

Gene flow is maintained by polyandry and male dispersal in the army ant <Emphasis Type="Italic">Eciton burchellii</Emphasis>

The combination of haplodiploidy, complementary sex determination and eusociality constrains the effective population size (N _e) of social Hymenoptera far more than in any other insect group. Additional limitations on N _e occur in army ants since they have wingless queens and colony fission, both of which are factors causing restricted maternal gene flow and high population viscosity. Therefore, winged army ant males gain a particular significance to ensure dispersal, facilitate gene flow and avoid inbreeding. Based on population genetic analyses with microsatellite markers, we studied a population of the Neotropical army ant Eciton burchellii, finding a high level of heterozygosity, weak population differentiation and no evidence for inbreeding. Moreover, by using sibship reconstruction analyses, we quantified the actual number of male contributing colonies represented in a queen’s mate sample, demonstrating that, through extreme multiple mating, the queens are able to sample the genes of males from up to ten different colonies, usually located within an approximate radius of 1 km. We finally correlated the individual mating success of each male contributing colony with the relative siring success of individual males and found a significant colony-dependent male fitness component. Our results imply that the dispersal and mating system of these army ants seem to enhance gene flow and minimise the deleterious effects associated with small effective population size. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants

The unique nomadic life-history pattern of army ants (army ant adaptive syndrome), including obligate colony fission and strongly male-biased sex-ratios, makes army ants prone to heavily reduced effective population sizes (N _e). Excessive multiple mating by queens (polyandry) has been suggested to compensate these negative effects by increasing genetic variance in colonies and populations. However, the combined effects and evolutionary consequences of polyandry and army ant life history on genetic colony and population structure have only been studied in a few selected species. Here we provide new genetic data on paternity frequencies, colony structure and paternity skew for the five Neotropical army ants Eciton mexicanum, E. vagans, Labidus coecus, L. praedator and Nomamyrmex esenbeckii; and compare those data among a total of nine army ant species (including literature data). The number of effective matings per queen ranged from about 6 up to 25 in our tested species, and we show that such extreme polyandry is in two ways highly adaptive. First, given the detected low intracolonial relatedness and population differentiation extreme polyandry may counteract inbreeding and low N _e. Second, as indicated by a negative correlation of paternity frequency and paternity skew, queens maximize intracolonial genotypic variance by increasingly equalizing paternity shares with higher numbers of sires. Thus, extreme polyandry is not only an integral part of the army ant syndrome, but generally adaptive in social insects by improving genetic variance, even at the high end spectrum of mating frequencies.     

Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii

Inhibited dispersal, leading to reduced gene flow, threatens populations with inbreeding depression and local extinction. Fragmentation may be especially detrimental to social insects because inhibited gene flow has important consequences for cooperation and competition within and among colonies. Army ants have winged males and permanently wingless queens; these traits imply male‐biased dispersal. However, army ant colonies are obligately nomadic and have the potential to traverse landscapes. Eciton burchellii, the most regularly nomadic army ant, is a forest interior species: colony raiding activities are limited in the absence of forest cover. To examine whether nomadism and landscape (forest clearing and elevation) affect population genetic structure in a montane E. burchellii population, we reconstructed queen and male genotypes from 25 colonies at seven polymorphic microsatellite loci. Pairwise genetic distances among individuals were compared to pairwise geographical and resistance distances using regressions with permutations, partial Mantel tests and random forests analyses. Although there was no significant spatial genetic structure in queens or males in montane forest, dispersal may be male‐biased. We found significant isolation by landscape resistance for queens based on land cover (forest clearing), but not on elevation. Summed colony emigrations over the lifetime of the queen may contribute to gene flow in this species and forest clearing impedes these movements and subsequent gene dispersal. Further forest cover removal may increasingly inhibit Eciton burchellii colony dispersal. We recommend maintaining habitat connectivity in tropical forests to promote population persistence for this keystone species.     

The structured diversity of specialized gut symbionts of the New World army ants

Symbiotic bacteria play important roles in the biology of their arthropod hosts. Yet the microbiota of many diverse and influential groups remain understudied, resulting in a paucity of information on the fidelities and histories of these associations. Motivated by prior findings from a smaller scale, 16S rRNA‐based study, we conducted a broad phylogenetic and geographic survey of microbial communities in the ecologically dominant New World army ants (Formicidae: Dorylinae). Amplicon sequencing of the 16S rRNA gene across 28 species spanning the five New World genera showed that the microbial communities of army ants consist of very few common and abundant bacterial species. The two most abundant microbes, referred to as Unclassified Firmicutes and Unclassified Entomoplasmatales, appear to be specialized army ant associates that dominate microbial communities in the gut lumen of three host genera, Eciton, Labidus and Nomamyrmex. Both are present in other army ant genera, including those from the Old World, suggesting that army ant symbioses date back to the Cretaceous. Extensive sequencing of bacterial protein‐coding genes revealed multiple strains of these symbionts coexisting within colonies, but seldom within the same individual ant. Bacterial strains formed multiple host species‐specific lineages on phylogenies, which often grouped strains from distant geographic locations. These patterns deviate from those seen in other social insects and raise intriguing questions about the influence of army ant colony swarm‐founding and within‐colony genetic diversity on strain coexistence, and the effects of hosting a diverse suite of symbiont strains on colony ecology.     

7. SHORT NOTES

Randall, R. and Ross, G. J. B. 1979. Increasing population of Cape Gannets on Bird Island, Algoa Bay, and observations on breeding success. Ostrich 50:168-175.

The South African Gannet Sula capensis on Bird Island has doubled in numbers between 1956 and 1974 and the process is continuing. The increase is similar to that of the two closely related species S. serrator and S. bassana. We estimated from the colony surface area and nest density that the number of birds with nests in 1974/5 was approximately 77 000. Making allowance for non-breeders, there were about 100 000 adults in 1974/5. Guano harvests from 1938–75 show considerable annual fluctuations with an overall downward trend. Poor agreement was found when relating guano harvests to population estimates, when the latter are gauged by colony surface area. We suggest that guano harvests are not good indicators of gannet population trends on Bird Island, primarily because of harvesting methods and environmental conditions. The number of chicks which fledged in the 1976/7 season in a section of the colony was far fewer than expected, even when allowances were made for egg-loss and chick mortality. A combination of heavier-than-usual rainfall and poor management techniques have resulted in high egg-loss and low chick numbers.     

Eight highly polymorphic microsatellite markers for the army ant Eciton burchellii

The army ant Eciton burchellii is a nomadic predator in the rain forests of Central and South America. Detailed work has documented many aspects of this species’ ecology, behaviour and life history. However, a detailed investigation into within colony relatedness structure requires the development of genetic tools. Here we present eight microsatellite markers with between nine and 25 alleles. For each loci there is close agreement between observed and expected heterozygosity.     

Colony fusion and worker reproduction after queen loss in army ants

Theory predicts that altruism is only evolutionarily stable if it is preferentially directed towards relatives, so that any such behaviour towards seemingly unrelated individuals requires scrutiny. Queenless army ant colonies, which have anecdotally been reported to fuse with queenright foreign colonies, are such an enigmatic case. Here we combine experimental queen removal with population genetics and cuticular chemistry analyses to show that colonies of the African army ant Dorylus molestus frequently merge with neighbouring colonies after queen loss. Merging colonies often have no direct co-ancestry, but are on average probably distantly related because of overall population viscosity. The alternative of male production by orphaned workers appears to be so inefficient that residual inclusive fitness of orphaned workers might be maximized by indiscriminately merging with neighbouring colonies to increase their reproductive success. We show that worker chemical recognition profiles remain similar after queen loss, but rapidly change into a mixed colony Gestalt odour after fusion, consistent with indiscriminate acceptance of alien workers that are no longer aggressive. We hypothesize that colony fusion after queen loss might be more widespread, especially in spatially structured populations of social insects where worker reproduction is not profitable.     

Effects of anthropogenic food resources on yellow-legged gull colony size on Mediterranean islands

Yellow-legged gull Larus michahellis populations have been studied on three archipelagos consisting of 20 islands distributed along 80 km of the French Mediterranean coastline. Population changes were analyzed between 1920 and 2006. In the first decades following their settlement on these islands, the yellow-legged gull populations showed a continuous exponential growth in the three archipelagos, in agreement with an annual geometric growth rate λ above 1. The population growth ceased to fit this model during the 1980s for the older colonies (Riou and Hyères Islands archipelagos). Thus, we focused on population changes occurring during the period 1982–2000, a pivotal period for which we have both precise census and anthropogenic food resource data, in order to determine environmental factors influencing these population changes using multiple linear regression models. An average annual growth rate of colony size was 1.02 for the last two decades. The changes in landfill availability, the gull density in 1982, and the nesting area in 1982 explained 84.4% of variation in colony size changes between 1982 and 2000. The yellow-legged gull changes on the islands in the last two decades increased as availability in anthropogenic food resources increased near the colony (positive ΔK). As a consequence, given no reduction in landfill activity or in accessibility for gulls, we expect this region to sustain continuous species expansion in the future.     

A discrete,stochastic model of colonial phytoplankton population size structure: Development and application to in situ imaging-in-flow cytometer observations of Dinobryon

The scientific community lacks models for the dynamic changes in population size structure that occur in colonial phytoplankton. This is surprising, as size is a key trait affecting many aspects of phytoplankton ecology, and colonial forms are very common. We aim to fill this gap with a new discrete, stochastic model of dynamic changes in phytoplankton colonies' population size structure. We use the colonial phytoplankton Dinobryon as a proof-of-concept organism. The model includes four stochastic functions—division, stomatocyst production, colony breakage, and colony loss—to determine Dinobryon population size structure and populations counts. Although the functions presented here are tailored to Dinobryon, the model is readily adaptable to represent other colonial taxa. We demonstrate how fitting our model to in situ observations of colony population size structure can provide a powerful approach to explore colony size dynamics. Here, we have (1) collected high-frequency in situ observations of Dinobryon in Lac (Lake) Montjoie (Quebec, Canada) in 2013 with a moored Imaging FlowCytobot (IFCB) and (2) fit the model to those observations with a genetic algorithm solver that extracts parameter estimates for each of the four stochastic functions. As an example of the power of this model-data integration, we also highlight ecological insights into Dinobryon colony size and stomatocyst production. The Dinobryon population was enriched in larger, flagellate-rich colonies near bloom initiation and shifted to smaller and emptier colonies toward bloom decline.     

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.     

Six weeks in the life of a reproducing army ant colony: male parentage and colony behaviour

The army ant Eciton burchellii is one of the most conspicuous ant species in New World tropical forests, but studies of colony life histories have been hampered by the nomadic lifestyle of these ants, which alternate between a nomadic phase when the colony relocates frequently, and a statary phase when the colony remains at a fixed site. Here we report on a colony from Venezuela that we studied continuously for six weeks, from the time that the queen produced a reproductive brood until the adult reproductives emerged and the colony entered the next cycle. Our findings support the contention that reproductive larvae develop faster than worker larvae, and that the nomadic phases of colonies with reproductive broods are significantly shorter than those of colonies with worker broods. This strongly suggests that the onset of pupation is linked to the onset of the statary phase. We used microsatellite genotyping to accurately identify male and queen larvae and we describe how they can be distinguished morphologically. Using the same genetic markers, we determined the parentage of 81 males produced by this colony. Only one of the males had a genotype that could not be directly derived from the observed queen genotype, but this mismatch is most probably due to a single mutation at one of the microsatellite loci, rather than this male being a worker son. We therefore conclude that this colony provides no evidence that workers lay eggs that develop into adult males in the presence of the queen, confirming the results of an earlier study on male parentage in an Old World army ant. Received 16 November 2006; revised 15 January 2007; accepted 16 January 2007.     

Effect of retentive markers on the dynamics of settlement: The case of arthropod silk

During a settlement decision, the presence of conspecifics is crucial to species subject to Allee effects, for which the number of founders affects the subsequent growth of the colony. Marking the area (physically or chemically) conveys information about the number of conspecifics present in a new patch. Here, we study how an individual affinity for the marker affects the dynamics of a foundation process. A generic population model is presented, in which marking and affinity for the marker are at stake. Our results show that population size thresholds can appear, below which settlement is not possible. This model is then used to study the dynamics of migration and aggregation in a set of interconnected populations. We show that affinity for the marker can induce asymmetries in the population distribution. Anelosimus eximius is a social spider subject to Allee effects, for which silk potentially acts as a marker. We test our predictions with field experiments involving two populations of A. eximius in a Y-shaped setup. The agreement between our experimental and theoretical results strongly supports the validity of the model. This allows us to use the model to estimate a realistic set of parameters of biological significance to this social spider.     

A method to assess population changes in king penguins: the use of a Geographical Information System to estimate area-population relationships

During the last decades, king penguin (Aptenodytes patagonicus) populations have been reported to increase throughout most of their breeding range. In this study, we compared the results obtained from direct counts of incubating king penguins with the results yielded by the estimation of the change in area occupied by breeding birds at the Ratmanoff king penguin colony at the Kerguelen Islands. The area of the colony was determined using a Geographical Information System with a georeferencing extension on aerial pictures taken in 1963, 1985 and 1998. Individual king penguin were counted on the same pictures or pictures taken on the same day. The overall population increase between 1963 and 1998 was 733% while the colony area increased by 677%. This study indicates that monitoring change in colony size is a good indicator for detecting and monitoring large population changes in king penguins, in particular for remote colonies. The discrepancy between the two results may be from two different kinds of bias. Firstly, there could be a possible error in the estimation of the area occupied by the colony resulting from the georeferencing of oblique pictures, and secondly, the density of king penguins may also change with population number. This method, which only requires high-altitude pictures, also reduces the possible disturbance to breeding made by low- to medium-altitude flights. Accepted: 7 February 2000     

Distribution of nucleotide differences between two randomly chosen cistrons in a subdivided population: The finite island model

Using the island model of finite size, the distributions as well as the means and variances of d_w and d_b are obtained, where d_w is the number of nucleotide differences between two cistrons randomly chosen from the same colony and d_b is the corresponding number between two cistrons randomly chosen from different colonies. The rate for the means to approach equilibrium is independent of mutation while that for the variances is somewhat retarded by mutation. At the steady state, the mean of d_w is independent of population subdivision and migration rate, as long as there is migration. It has been shown that the actual genic variation in a colony may be much larger than that revealed by the heterozygosity in the colony.     

Serial monodomy in ants: an antipredator strategy?

Abstract.  1. The term serial monodomy is used to describe a life-history phenomenon in social insects. Serially monodomous colonies maintain multiple nests for their exclusive use, but only occupy one nest at a time.
2. The hypothesis that colony odours mediate nest relocation decisions was tested in the serially monodomous species Aphaenogaster araneoides from Central America. Odour extracts of colony members were created using a non-polar solvent.
3. Colonies strongly avoided reoccupying nests treated with colony odour extracts, while control colonies often returned to nests subjected to solvent-only control. Behavioural observations indicated that A. araneoides colonies are capable of detecting army ant ( Eciton burchellii ) raids up to 1.4 m from the raiding front, with several seconds to evacuate nests.
4. It is proposed that the function of serial monodomy in A. araneoides is the reduction of nest odour to enhance detection of predaceous army ants. Serial monodomy may be a widespread but undocumented mode of nesting where army ants occur in tropical and subtropical climates.     

Crossfostered drones ofApis cerana (Fabricius, 1793) andApis koschevnikovi (Buttel-Reepen, 1906) fly at their species specific mating times

Summary Reciprocal transfer of sealed drone brood between colonies ofApis cerana andApis koschevnikovi was successful and resulted in four colonies (two of each species) with a mixed drone population. Flights ofApis cerana drones occurred between 14.00 and 16.15 regardless whether they were in a conspecific or alien colony.Apis koschevnikovi drones also flew at their species specific time from 16.45 to 18.30. A variance estimation revealed that 99.4% of the total variance depended on the species of the drone. In contrast to theApis drone's general biological dependence upon the colony, crossfostered drones ofApis cerana andApis koschevnikovi showed an unexpected autonomy in chosing their mating flight time.     

Predicting order of conformational changes during protein conformational transitions using an interpolated elastic network model

The decryption of sequence of structural events during protein conformational transitions is essential to a detailed understanding of molecular functions ofvarious biological nanomachines. Coarse‐grained models have proven useful by allowing highly efficient simulations of protein conformational dynamics. By combining two coarse‐grained elastic network models constructed based on the beginning and end conformations of a transition, we have developed an interpolated elastic network model to generate a transition pathway between the two protein conformations. For validation, we have predicted the order of local and global conformational changes during key ATP‐driven transitions in three important biological nanomachines (myosin, F₁ ATPase and chaperonin GroEL). We have found that the local conformational change associated with the closing of active site precedes the global conformational change leading to mechanical motions. Our finding is in good agreement with the distribution of intermediate experimental structures, and it supports the importance of local motions at active site to drive or gate various conformational transitions underlying the workings of a diverse range of biological nanomachines. Proteins 2010. © 2010 Wiley‐Liss, Inc.     

Directional raids by army ants as an adaption to patchily distributed food: a simulation model

A typical colony of Neotropical army ants (subfamily Ecitoninae) regularly raids a large area around their bivouac by forming a narrow directional column that can reach up to one hundred meters in length. The raid is finished and then relaunched 12–17 times, each time toward different orientation. After completing all bouts the colony relocates to a new area. A hypothetical alternative to this foraging mode is raiding radially and symmetrically by expanding the search front in every direction like a circular bubble. Using an existing agent-based modeling software that simulates army ants’ behavior, we compared the two possible modes of foraging in different food distributions. Regardless of the food patch abundance, the radial raiding was superior to the directional raiding when food patches had low quality, and the directional raiding was favorable when the patches were rich. In terms of energy efficiency, the radial raiding was the better strategy in a wide range of conditions. In contrast, the directional raiding tended to yield more food per coverage area. Based on our model, we suggest that the directional raiding by army ants is an adaptation to the habitats with abundance of high-quality food patches. This conclusion fits well with the ecology of army ants.