Jürgen Heinze

The genome of the fire ant Solenopsis invicta

Ants have evolved very complex societies and are key ecosystem members. Some ants, such as the fire ant Solenopsis invicta, are also major pests. Here, we present a draft genome of S. invicta, assembled from Roche 454 and Illumina sequencing reads obtained from a focal haploid male and his brothers. We used comparative genomic methods to obtain insight into the unique features of the S. invicta genome. For example, we found that this genome harbors four adjacent copies of vitellogenin. A phylogenetic analysis revealed that an ancestral vitellogenin gene first underwent a duplication that was followed by possibly independent duplications of each of the daughter vitellogenins. The vitellogenin genes have undergone subfunctionalization with queen- and worker-specific expression, possibly reflecting differential selection acting on the queen and worker castes. Additionally, we identified more than 400 putative olfactory receptors of which at least 297 are intact. This represents the largest repertoire reported so far in insects. S. invicta also harbors an expansion of a specific family of lipid-processing genes, two putative orthologs to the transformer/feminizer sex differentiation gene, a functional DNA methylation system, and a single putative telomerase ortholog. EST data indicate that this S. invicta telomerase ortholog has at least four spliceforms that differ in their use of two sets of mutually exclusive exons. Some of these and other unique aspects of the fire ant genome are likely linked to the complex social behavior of this species.

Alternative reproductive strategies: a queen perspective in ants

Ant colonies are commonly thought to have a stable and simple family structure, with one or a few egg-laying queens and their worker daughters. However, recent genetic studies reveal that the identity of breeding queens can vary over time within colonies. In several species, some queens are apparently specialized to enter established colonies instead of initiating a new colony on their own. The previously overlooked occurrence of queen turnover within colonies has important consequences not only on the genetic structure and nature of kin conflict within colonies, but also on the evolution of social parasitism.

Ant reproductive strategies

In contrast to what is generally believed, the reproductive strategies of ants are remarkably diverse and include such different phenomena, as wingless female and male sexuals, reproduction by mated workers, thelytokous parthenogenesis, and complete workerlessness. We review the various reproductive life histories and investigate them in the light of recent models on the evolution of dispersal strategies and multiple-queening. It appears that most deviations from “normal” colony propagation can be explained by a decreased success of dispersal and solitary founding by solitary queens in certain types of habitats. Consequently, alternative reproductive strategies are found especially in those species, in which environmental conditions or a highly specialized way of life are thought to make solitary founding costly. Among the key factors, which determine the success of reproductive strategies, appear to be spatial and temporal distribution of habitats and the availability of nest sites.

Does she smell like a queen? Chemoreception of a cuticular hydrocarbon signal in the ant Pachycondyla inversa

SUMMARY Primitive ant societies, with their relatively simple social structure, provide an opportunity to explore the evolution of chemical communication, in particular of mechanisms underlying within-colony discrimination. In the same colony, slight differences in individual odours can be the basis for discrimination between different castes, classes of age and social status. There is some evidence from correlative studies that such inter-individual variation is associated with differences in reproductive status, but direct proof that certain chemical compounds are detected and recognized by ants is still lacking. In the ponerine ant Pachycondyla inversa, fertile queens and, in orphaned colonies, dominant egg-laying workers are characterized by the predominance of a branched hydrocarbon, 3,11-dimethylheptacosane (3,11-diMeC27) on the cuticle. Using electroanntennography and gas chromatography with electroantennographic detection, we show that the antennae of P. inversa workers react to this key compound. 3,11-diMeC27 is correlated with ovarian activity and, because it is detected, is likely to assume the role of a fertility signal reflecting the quality of the sender.

Moribund Ants Leave Their Nests to Die in Social Isolation

Animal societies provide perfect conditions for the spread of infections and are therefore expected to employ mechanisms that reduce the probability of transmitting pathogens to group members [1-4]. Death in nature rarely results from old age but commonly results from diseases. Leaving ones group to die in seclusion might be an efficient way of minimizing the risk of infecting kin. Anecdotal observations of moribund individuals deserting from their groups exist for several species, including humans (e.g., [5]), but have rarely been substantiated by quantitative analysis. Furthermore, to confirm that dying in solitude has evolved because of its altruistic benefits requires refuting the alternative explanation of pathogen manipulation of host behavior. Here we show that workers of the ant Temnothorax unifasciatus dying from fungal infection, uninfected workers whose life expectancy was reduced by exposure to 95% CO(2)[6, 7], and workers dying spontaneously in observation colonies exhibited the same suite of behavior of isolating themselves from their nestmates days or hours before death. Actively leaving the nest and breaking off all social interactions thus occurred regardless of whether individuals were infected or not. Social withdrawal might be a commonly overlooked altruistic trait serving the inclusive fitness interests of dying individuals in social animals.

Worker rank, reproductive status and cuticular hydrocarbon signature in the ant, Pachycondyla cf. inversa

Abstract. Workers in de-queened colonies of the neotropical ant, Pachycondyla cf. inversa, form linear or near-linear dominance hierarchies by violent antennation and biting. In these rank orders, social status and ovarian activity are on average highly correlated. Whereas the presence of a fertile queen appears to be sufficient to prevent workers from laying eggs, fertile workers do not completely control reproduction by their nestmates, suggesting that workers are able to differentiate between an egg-laying queen and an egg-laying worker. Here we show that the composition of cuticular hydrocarbons of egg-laying workers is quantitatively and qualitatively different from that of non-laying workers and resembles the hydrocarbon blend of the queen but does not completely match it. Furthermore, using discriminant analysis, it was possible to distinguish workers with four different classes of ovarian development based only on their cuticular hydrocarbon profiles. Fertility-associated changes in cuticular hydrocarbons may play an important role in the behavioural regulation of reproduction in this ant.

Worker policing without genetic conflicts in a clonal ant

In group-living animals, mutual policing to suppress reproduction is an important mechanism in the resolution of conflict between selfish group members and the group as a whole. In societies of bees, ants, and wasps, policing against the production of males by other workers is expected when egg laying by workers decreases the average inclusive fitness of individual group members. This may result (i) from the relatedness of workers being lower to workerthan to queen-derived males or (ii) from a lowered overall colony efficiency. Whereas good evidence exists for policing behavior caused by genetic conflicts, policing caused by efficiency factors has not been demonstrated. We investigated the regulation of reproduction in the ant Platythyrea punctata, a species in which colonies are clones because workers are capable of producing female offspring by thelytokous parthenogenesis. Reproductive conflicts resulting from differences in genetic relatedness are therefore not expected, but uncontrolled reproduction by all workers could lead to the destruction of sociality. Here we show that worker policing by aggressive attacks against additionally reproducing workers keeps the number of reproducing workers low. Furthermore, through experimental manipulation of the number of brood items per colony, we show that worker policing can enhance group efficiency.

Conflict and cooperation in ant societies

We review the different levels of reproductive conflict within ant societies. Workers and queens may disagree about sex allocation and the origin of males. Other conflicts arise between queens in multiply queened colonies and occasionally also between workers. These conflicts are resolved either by manipulation, such as sexual deception, changed mating patterns, or pheromonal signaling, or by physical aggression among nestmates. We outline the conditions under which physical aggression occurs and which behaviors are involved in the regulation of reproductive dominance.

Individual Recognition in Ant Queens

Personal relationships are the cornerstone of vertebrate societies, but insect societies are either too large for individual recognition, or their members were assumed to lack the necessary cognitive abilities . This paradigm has been challenged by the recent discovery that paper wasps recognize each others unique facial color patterns . Individual recognition is advantageous when dominance hierarchies control the partitioning of work and reproduction . Here, we show that unrelated founding queens of the ant Pachycondyla villosa use chemical cues to recognize each other individually. Aggression was significantly lower in pairs of queens that had previously interacted than in pairs with similar social history but no experience with one another. Moreover, subordinates discriminated familiar and unfamiliar dominants in choice experiments in which physical contact, but not odor perception, was prevented and in tests with anaesthetized queens. The cuticular chemical profiles of queens were neither associated with dominance nor fertility and, therefore, do not represent status badges , and nestmate queens did not share a common odor. Personal recognition facilitates the maintenance of stable dominance hierarchies in these small societies. This suggests that the ability to discriminate between individual traits is selected for when it incurs net benefits for the resolution of conflict.

Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi

Most social Hymenoptera are characterized by simple haploid sex determination and environment-based caste differentiation. This appears to be strikingly different in the queen-polymorphic ant Vollenhovia emeryi. Almost all long- and short-winged queens from a population in Central Japan were homozygous at three microsatellite loci, whereas workers were mostly heterozygous, suggesting either a complex system of genetic caste determination or, more likely, the production of female sexuals from unfertilized eggs by thelytokous parthenogenesis and of workers from fertilized eggs. Furthermore, male genotypes were not compatible with those of the queens and had exclusively the paternal allele found in the sterile, heterozygous workers, probably because males are produced from fertilized eggs after the exclusion of maternal nuclear DNA as recently reported for Wasmannia auropunctata. The genus Vollenhovia might provide an interesting model system to trace the evolution of unusual caste and sex determination systems.