Worker caste determination in the army ant Eciton burchellii

Elaborate division of labour has contributed significantly to the ecological success of social insects. Division of labour is achieved either by behavioural task specialization or by morphological specialization of colony members. In physical caste systems, the diet and rearing environment of developing larvae is known to determine the phenotype of adult individuals, but recent studies have shown that genetic components also contribute to the determination of worker caste. One of the most extreme cases of worker caste differentiation occurs in the army ant genus Eciton, where queens mate with many males and colonies are therefore composed of numerous full-sister subfamilies. This high intracolonial genetic diversity, in combination with the extreme caste polymorphism, provides an excellent test system for studying the extent to which caste determination is genetically controlled. Here we show that genetic effects contribute significantly to worker caste fate in Eciton burchellii. We conclude that the combination of polyandry and genetic variation for caste determination may have facilitated the evolution of worker caste diversity in some lineages of social insects.     

The foraging ecology of the army ant Eciton rapax: an ergonomic enigma?

Abstract. 1. The army ant Eciton rapax (F. Smith) produces longer raid systems than any other member of its genus and it is a specialist predator of forest floor and understory ants such as species of Camponotus, Odontomachus and Pachycondyla.
2. Allometrical analysis confirms that E. rapax is the only member of its genus without distinct physical castes among its workers: its foraging population is entirely monomorphic and there are no majors.
3. The workers of E. rapax are distributed over a considerable size range, and there are distinct divisions of labour within these colonies: small workers tend to stay in the nests and among the larger foraging workers those retrieving prey items are significantly bigger than the rest.
4. An analysis of foraging efficiency and worker performance in E. rapax suggests that transport costs, resulting from the great distances that workers travel during raids and emigrations, are one of the selection pressures that have favoured the evolution of large monomorphic workers in this species.     

Predation and patchiness in the tropical litter: do swarm-raiding army ants skim the cream or drain the bottle?

1. Swarm-raiding army ants have long been considered as episodic, catastrophic agents of disturbance in the tropical litter, but few quantitative data exist on their diets, preferences, and, critically, their ability to deplete prey. 2. Here, we provide such data for two common species of swarm raiders broadly sympatric throughout the Neotropics: the iconic Eciton burchellii and the more secretive, less studied Labidus praedator. In Ecuador, Costa Rica, Venezuela and Panama, patches of forest floor were sampled for litter invertebrates immediately before and after army ant raids. These invertebrates have been shown to regulate decomposition and vary 100-fold in local densities across the forest floor. 3. Contrary to Eciton's popular image, only Labidus consistently reduced the biomass of litter invertebrates and only then by an average of 25%. Eciton's impacts were concentrated on rich patches of invertebrates, while Labidus prey depletion showed no such density dependence. Labidus reduced the biomass of some invertebrates-isopods, larviforms and coleoptera-by up to 75%; Eciton showed no such prey preferences. 4. Our results suggest that Eciton specializes on high biomass patches, while Labidus feeds profitably from any litter patch. Combined, these swarm raiders sum to be chronic, but not catastrophic, predators of common litter invertebrates of the brown food web.     

Novel approach to heritability detection suggests robustness to paternal genotype in a complex morphological trait

Heritable variation is essential for evolution by natural selection. In Neotropical army ants, the ecological role of a given species is linked intimately to the morphological variation within the sterile worker caste. Furthermore, the army ant Eciton burchellii is highly polyandrous, presenting a unique opportunity to explore heritability of morphological traits among related workers sharing the same colonial environment. In order to exploit the features of this organismal system, we generated a large genetic and morphological dataset and applied our new method that employs geometric morphometrics (GM) to detect the heritability of complex morphological traits. After validating our approach with an existing dataset of known heritability, we simulated our ability to detect heritable variation given our sampled genotypes, demonstrating the method can robustly recover heritable variation of small effect size. Using this method, we tested for genetic caste determination and heritable morphological variation using genetic and morphological data on 216 individuals of E. burchellii. Results reveal this ant lineage (1) has the highest mating frequency known in ants, (2) demonstrates no paternal genetic caste determination, and (3) suggests a lack of heritable morphological variation in this complex trait associated with paternal genotype. We recommend this method for leveraging the increased resolution of GM data to explore and understand heritable morphological variation in nonmodel organisms.     

Geographic variation of caste structure among ant populations

Morphologically distinct worker castes of eusocial insects specialize in different tasks. The relative proportions of these castes and their body sizes represent the demography of a colony that is predicted to vary adaptively with environments. Despite strong theoretical foundations, there has been little empirical evidence for the evolution of colony demography in nature. We show that geographically distinct populations of the ant Pheidole morrisi differ in worker caste ratios and worker body sizes in a manner consistent with microevolutionary divergence. We further show that the developmental mechanism for caste determination accounts for the unique pattern of covariation observed in these two traits. Behavioral data reveal that the frequency of different tasks performed by workers changes in a caste-specific manner when caste ratios are altered and demonstrate the importance of the major caste in colony defense. The population-level variation documented here for P. morrisi colonies supports the predictions of adaptive demography theory and illustrates that developmental mechanisms can play a significant role in shaping the evolution of phenotype at the colony level.     

The Soldiers in Societies: Defense,Regulation, and Evolution

The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies. Adaptation and regulation of the sterile caste, to a certain extent, drives the evolution of eusociality. Depending on adaptive functions of the first evolved sterile caste, eusocial societies can be categorized into the worker-first and soldier-first lineages, respectively. The former is marked by a worker caste as the first evolved altruistic caste, whose primary function is housekeeping, and the latter is highlighted by a sterile soldier caste as the first evolved altruistic caste, whose task is predominantly colony defense. The apparent functional differences between these two fundamentally important castes suggest worker-first and soldier-first eusociality are potentially driven by a suite of distinctively different factors. Current studies of eusocial evolution have been focused largely on the worker-first Hymenoptera, whereas understanding of soldier-first lineages including termites, eusocial aphids, gall-dwelling thrips, and snapping shrimp, is greatly lacking. In this review, we summarize the current state of knowledge on biology, morphology, adaptive functions, and caste regulation of the soldier caste. In addition, we discuss the biological, ecological and genetic factors that might contribute to the evolution of distinct caste systems within eusocial lineages.     

Method Review: Estimation of Colony Densities of the Army Ant Eciton burchellii in Costa Rica

We evaluated the performance of a method developed to estimate colony densities of the army ant Eciton burchellii , a keystone species, based on raid crossings on trails, in Costa Rica. The method was compared with a census obtained by tracking ant-following birds, and the effect of walking distance and rainfall was evaluated. We found that the method performs well when at least 60 km of trail have been walked (replicated walks are permissible), and when rainfall is avoided.     

The blind leading the blind in army ant raid patterns: Testing a model of self-organization (Hymenoptera: Formicidae)

We present field experiments and analyses that test both the assumptions and the predictions of a model that showed how the swarm raids of the army ant Eciton burchellimight be self-organizing, i.e., based on hundreds of thousands of interactions among the foraging workers rather than a central administration or hierarchical control. We use circular mill experiments to show that the running velocity of the ants is a sigmoidal function of the strength of their trail pheromones and provide evidence that the swarm raid is structured by the interaction between outbound and inbound forager traffic mediated by the pheromones produced by both of these sets of ants. Inbound traffic is also affected by the distribution of prey, and hence, sites of prey capture alter the geometry of the raid. By manipulating the prey distributions for E. burchelliswarms, we have made them raid in a form more typical of other army ant species. Such self-organization of raids based on an interaction between the ants and their environment has profound consequences for interpretations of the evolution of army ant species.     

The effects of kin selection on rates of molecular evolution in social insects

The evolution of sociality represented a major transition point in biological history. The most advanced societies, such as those displayed by social insects, consist of reproductive and nonreproductive castes. The caste system fundamentally affects the way natural selection operates. Specifically, selection acts directly on reproductive castes, such as queens, but only indirectly through the process of kin selection on nonreproductive castes, such as workers. In this study, we present theoretical analyses to determine the rate of substitution at loci expressed exclusively in the queen or worker castes. We show that the rate of substitution is the same for queen- and worker-selected loci when the queen is singly mated. In contrast, when a queen is multiply mated, queen-selected loci show higher rates of substitution for adaptive alleles and lower rates of substitution for deleterious alleles than worker-selected loci. We compare our theoretical expectations to previously obtained genomic data from the honeybee, Apis mellifera, where queens mate multiply and the fire ant, Solenopsis invicta, where queens mate singly and find that rates of evolution of queen- and worker-selected loci are consistent with our predictions. Overall, our research tests theoretical expectations using empirically obtained genomic data to better understand the evolution of advanced societies.     

Physiology as a caste-defining feature

Division of labour is a key factor in the ecological success of social insects. Groups of individuals specializing on a particular behaviour are known as castes and are usually distinguished by morphology or age. Physiology plays a key role in both these types of caste, in either the developmental physiology which determines morphology, or the temporal changes in physiology over an insect’s life. Physiological correlates of morphological or temporal caste include differences in gland structure, secretory products, leanness, neuroanatomy and neurochemistry. However, purely physiological castes could also occur. Physiological castes are discrete groups of same-age same-size individuals with particular physiological competencies, or groups of individuals with similar physiology crossing age or size groups. A stable physiological caste occurs in the monomorphic Pharaoh’s ant, where some ants can detect old pheromone trails and retain this specialization over time. These ants differ physiologically from other workers, and the differences arise before eclosion. More temporary physiological castes occur in the ant Ectatomma where brood care specialists have more developed ovarioles than other same-aged workers, and in the honeybee where nurses, wax-workers and soldiers all differ physiologically from same-aged nestmates. Physiology is an important aspect of caste, not only in its contribution to age-related and morphological castes, but also in its own right as a caste grouping factor. While age and morphological differences make caste structures accessible for study, more cryptic physiological castes may play just as important a role in division of labour. Received 19 December 2007; revised 24 July and 18 September 2008; accepted 19 September 2008.     

Birds and army ants in a fragment of the Atlantic Forest of Brazil

ABSTRACT Little is known about the birds associated with army‐ant swarms in the Brazilian Atlantic forest. Our objectives were to locate and monitor army‐ant swarms in the Atlantic rainforest of Brazil and to identify the species of birds that attended the swarms and exhibited bivouac‐checking behavior. From July 2004 to August 2005, we located 49 swarms of army ants, including 28 Eciton burchelli, 19 Labidus praedator, and 2 Eciton vagans swarms. No birds were present at 17 (35%) swarms. At 32 swarms where birds were present, 22 (69%) were E. burchelli swarms and 10 (31%) were L. praedator swarms. No birds were observed at the two E. vagans swarms. We identified 66 species of birds attending the swarms, but only 43 species were observed foraging on prey flushed by the ants. Eighteen of these species had not been previously reported to forage in association with army‐ant swarms. Most birds observed during our study attended army‐ant swarms opportunistically, with White‐shouldered Fire‐eyes (Pyriglena leucoptera) the only obligate ant follower. Our observations suggest that the arthropods and other organisms flushed by army ants represent an important food resource for several species of birds in the Atlantic forest ecosystem.     

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.     

Social organization in a flatworm: trematode parasites form soldier and reproductive castes

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of ‘parthenitae’ within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the ‘recognition of self’ and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.     

Caste‐biases in gene expression are specific to developmental stage in the ant Formica exsecta

Understanding how a single genome creates and maintains distinct phenotypes is a central goal in evolutionary biology. Social insects are a striking example of co‐opted genetic backgrounds giving rise to dramatically different phenotypes, such as queen and worker castes. A conserved set of molecular pathways, previously envisioned as a set of ‘toolkit’ genes, has been hypothesized to underlie queen and worker phenotypes in independently evolved social insect lineages. Here, we investigated the toolkit from a developmental point of view, using RNA‐Seq to compare caste‐biased gene expression patterns across three life stages (pupae, emerging adult and old adult) and two female castes (queens and workers) in the ant Formica exsecta. We found that the number of genes with caste‐biased expression increases dramatically from pupal to old adult stages. This result suggests that phenotypic differences between queens and workers at the pupal stage may derive from a relatively low number of caste‐biased genes, compared to higher number of genes required to maintain caste differences at the adult stage. Gene expression patterns were more similar among castes within developmental stages than within castes despite the extensive phenotypic differences between queens and workers. Caste‐biased expression was highly variable among life stages at the level of single genes, but more consistent when gene functions (gene ontology terms) were investigated. Finally, we found that a large part of putative toolkit genes were caste‐biased at least in some life stages in F. exsecta, and the caste‐biases, but not their direction, were more often shared between F. exsecta and other ant species than between F. exsecta and bees. Our results indicate that gene expression should be examined across several developmental stages to fully reveal the genetic basis of polyphenisms.     

Caste specialization in behavioral defenses against fungus garden parasites in <Emphasis Type="Italic">Acromyrmex octospinosus</Emphasis> leaf-cutting ants

Division of labor and caste specialization plays an important role in many aspects of social insect colony organization, including parasite defense. Within leaf-cutting ant colonies, worker caste specialization permeates colony tasks ranging from foraging, substrate incorporation, brood care, and chemical defenses via glandular secretions and mutualistic bacteria. Leaf-cutting ants rely on protecting a mutualistic fungus they grow for food from microfungi in the genus Escovopsis that parasitizes the ant–fungus relationship. Here, we examine whether Acromyrmex octospinosus leaf-cutter ant castes (minors and majors) display task specialization in two behavioral defenses against Escovopsis: fungus grooming (the removal of Escovopsis spores) and weeding (the removal of large pieces of Escovopsis-infected fungus garden). Using behavioral observations, we show that minors are the primary caste that performs fungus grooming, while weeding is almost exclusively performed by majors. In addition, using a sub-colony infection experimental setup, we show that at the early stages of infection, minors more efficiently remove Escovopsis spores from the fungus garden, thereby restricting Escovopsis spore germination and growth. At later stages of infection, after Escovopsis spore germination, we find that major workers are as efficient as minors in defending the fungus garden, likely due to the increased importance of weeding. Finally, we show, using SEM imaging, that the number of sensory structures is similar between minor and major workers. If these structures are invoked in recognition of the parasites, this finding suggests that both castes are able to sense Escovopsis. Our findings support that leaf-cutter ant behavioral defense tasks against Escovopsis are subject to caste specialization, likely facilitated by worker sizes being optimal for grooming and weeding by minors and majors, respectively, with important consequences for cultivar defense.     

Bigger Helpers in the Ant Cataglyphis bombycina: Increased Worker Polymorphism or Novel Soldier Caste?

Introduction

The mechanisms by which development favors or constrains the evolution of new phenotypes are incompletely understood. Polyphenic species may benefit from developmental plasticity not only regarding ecological advantages, but also potential for evolutionary diversification. For instance, the repeated evolution of novel castes in ants may have been facilitated by the existence of alternative queen and worker castes and their respective developmental programs.

Material and Methods

Cataglyphis bombycina is exceptional in its genus because winged queens and size-polymorphic workers occur together with bigger individuals having saber-shaped mandibles. We measured seven body parts in more than 150 individuals to perform a morphometric analysis and assess the developmental origin of this novel phenotype.

Results

Adults with saber-shaped mandibles differ from both workers and queens regarding the size of most body parts. Their relative growth rates are identical to workers for some pairs of body parts, and identical to queens for other pairs of body parts; critical sizes differ in all cases.

Conclusions

Big individuals are a third caste, i.e. soldiers, not major workers. Novel traits such as elongated mandibles are combined with a mix of queen and worker growth rates. We also reveal the existence of a dimorphism in the queen caste (microgynes and macrogynes). We discuss how novel phenotypes can evolve more readily in the context of an existing polyphenism. Both morphological traits and growth rules from existing queen and worker castes can be recombined, hence mosaic phenotypes are more likely to be viable. In C. bombycina, such a mosaic phenotype appears to function both for defense (saber-shaped mandibles) and fat storage (big abdomen). Recycling of developmental programs may have contributed to the morphological diversity and ecological success of ants.     

Queen,worker, and male yellowjacket wasps receive different nutrition during development

Nutritional variation among developing larvae is a long-standing hypothesis for how a sterile caste could evolve, with larvae deprived of nutrition becoming sterile or not leaving the nest. In this study, we test whether the three castes of the eusocial yellowjacket wasp (Vespula maculifrons) differ in the trophic source of their larval diet, their overall carbon (C) and nitrogen (N) content, as well as the distribution of C and N across body parts. Virgin queens (gynes) assimilated food from a higher relative trophic level compared to males, and workers were the lowest. Gynes, due to their much greater mass compared to the other castes are much more costly in terms of N, but males have the lowest C:N ratio. The variation in C:N is likely due to differences in life history between males and females (gynes and workers), where females invest more in energy storage (e.g., lipids) compared to males which have very short life spans; the major difference is in the abdomen, where fat is stored. The results of this study complement similar results in ants, which evolved a reproductive division of labor independently, and which diverged from vespid wasps near 150 million years ago. Similarities between how wasp and ant caste determination occurs suggest either a conserved mechanism that predates the evolution of eusociality or convergence on the same mechanism for generating alternative phenotypes. Provisioning N-expensive castes with food from a higher trophic level likely increases efficiency of N delivery because of N-enrichment with increasing trophic level.