Adrian A. Smith

Cuticular Hydrocarbons Reliably Identify Cheaters and Allow Enforcement of Altruism in a Social Insect

Cheaters are a threat to every society and therefore societies have established rules to punish these individuals in order to stabilize their social system. Recent models and observations suggest that enforcement of reproductive altruism (policing) in hymenopteran insect societies is a major force in maintaining high levels of cooperation. In order to be able to enforce altruism, reproductive cheaters need to be reliably identified. Strong correlational evidence indicates that cuticular hydrocarbons are the means of identifying cheaters, but direct proof is still missing. In the ant Aphaenogaster cockerelli, we mimicked reproductive cheaters by applying a synthetic compound typical of fertile individuals on nonreproductive workers. This treatment induced nestmate aggression in colonies where a queen was present. As expected, it failed to do so in colonies without a queen where workers had begun to reproduce. This provides the first direct evidence that cuticular hydrocarbons are the informational basis of policing behaviors, serving a major function in the regulation of reproduction in social insects. We suggest that even though cheaters would gain from suppressing these profiles, they are prevented from doing so through the mechanisms of hydrocarbon biosynthesis and its relation to reproductive physiology. Cheaters are identified through information that is inherently reliable.

Hydrocarbon Signals Explain the Pattern of Worker and Egg Policing in the Ant Aphaenogaster cockerelli

In ant societies, worker reproduction is regulated through policing behaviors, such as physical aggression or egg eating. The information used by policing individuals is thought to be in blends of hydrocarbons present on the cuticle and the surface of eggs. These fertility signals have been studied in numerous genera. However, signaling patterns that emerge across distinct subfamilies of ants have yet to be explained. We investigated policing behavior and the chemical signaling upon which policing behaviors are informed in the ant Aphaenogaster cockerelli. We found that worker-produced eggs are not policed, and we showed that there is a lack of chemical signaling for effective egg policing to occur in this species. Furthermore, we identified the available signals that demarcate workers to be policed physically. We showed that in A. cockerelli, a species with derived social organization, workers produce fertility signals identical to the queen. This queen-like signaling may be due to workers maintaining a high level of ovarian activity, linked to trophic egg production, in the presence of the queen.

Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus

Eusociality is characterized by a reproductive division of labor, wherein workers respond to the presence of reproductive individuals by refraining from reproduction themselves and restricting the reproductive efforts of others. Our understanding of how eusociality is maintained therefore depends on characterizing the mechanism by which workers detect the presence of a reproductive. Variations in cuticular hydrocarbons correspond to changes in reproductive ability in ants, and experimental studies are beginning to reveal the function of hydrocarbons as signals. In this study, we compare the cuticular hydrocarbon profiles of dominant and reproductive workers and queens of the ant Odontomachus brunneus with profiles of non-reproductive workers. Using split/reunification tests we document the existence of worker policing in both queenless and queenright colonies; supernumerary reproductives were treated aggressively by nestmates. Finally, we induce aggression and replicate queen-like submissive nestmate responses by supplementing the hydrocarbon profile of workers with (Z)-9-nonacosene, a compound that was significantly more abundant on the cuticles of reproductives. In three bioassays, we compare this manipulation to various control manipulations of the hydrocarbon profile and demonstrate that workers gauge the reproductive activity of nestmates through changes in their cuticular hydrocarbon profiles.

A conserved fertility signal despite population variation in the cuticular chemical profile of the trap-jaw ant Odontomachus brunneus.

SUMMARY Contact pheromones in the form of cuticular hydrocarbons are widespread among insects. Eusocial insects present a special challenge for understanding the evolution of the cuticular hydrocarbon profile because this blend is responsible for multiple distinct roles such as nestmate recognition and signalling fertility status. This study investigates these two signalling roles of the hydrocarbon profile in the trap-jaw ant Odontomachus brunneus. We demonstrate that the cuticular hydrocarbon profile is highly variable across populations and provide evidence that these differences are used for nestmate discrimination. Through manipulative experiments we also show that (Z)-9-nonacosene (Z9:C29) is used as a fertility signal and its role is conserved across populations. Our data demonstrate that both fertility and nestmate signalling influence the cuticular hydrocarbon profile and specifically the relative abundance of Z9:C29 on the cuticle of O. brunneus. Our study suggests that natural selection works on the cuticular chemical profile through multiple regulatory pathways, diversifying nestmate signals while conserving fertility signals.

Reclaiming the crown: queen to worker conflict over reproduction in Aphaenogaster cockerelli

In many social taxa, reproductively dominant individuals sometimes use aggression to secure and maintain reproductive status. In the social insects, queen aggression towards subordinate individuals or workers has been documented and is predicted to occur only in species with a small colony size and a low level of queen–worker dimorphism. We report queen aggression towards reproductive workers in the ant species Aphaenogaster cockerelli, a species with a relatively large colony size and a high level of reproductive dimorphism. Through analysis of cuticular hydrocarbon profiles, we show that queens are aggressive only to reproductively active workers. Non-reproductive workers treated with a hydrocarbon typical for reproductives are attacked by workers but not by queens, which suggests different ways of recognition. We provide possible explanations of why queen aggression is observed in this species.

Comparative analysis of fertility signals and sex-specific cuticular chemical profiles of Odontomachus trap-jaw ants

ABSTRACT The lipid mixture that coats the insect cuticle contains a number of chemical signals. Mate choice in solitary insects is mediated by sexually dimorphic cuticular chemistry, whereas in eusocial insects, these profiles provide information through which colony members are identified and the fertility status of individuals is assessed. Profiles of queens and workers have been described for a number of eusocial species, but there have been few comparisons of fertility signals among closely related species. Additionally, sexual dimorphism in cuticular lipid profiles has only been reported in two species of ants. This study describes the cuticular chemical profiles of queens, workers and males of three species of Odontomachus trap-jaw ants: O. ruginodis, O. relictus and O. haematodus. These are compared with fertility signals and sexually dimorphic profiles already described from O. brunneus. We report that fertility signals are not conserved within this genus: chemical compounds that distinguish queens from workers vary in number and type among the species. Furthermore, the compounds that were most abundant in cuticular extracts of O. ruginodis queens relative to workers were novel 2,5-dialkyltetrahydrofurans. Bioassays of extracts of O. ruginodis queens indicate that the dialkyltetrahydrofuran and hydrocarbon fractions of the profile are likely to work synergistically in eliciting behavioral responses from workers. In contrast, cuticular lipids that distinguish males from females are more conserved across species, with isomeric and relative abundance variations comprising the main differences among species. Our results provide new insights into how these contact chemical signals may have arisen and evolved within eusocial insects. Highlighted Article: Fertility signals are not conserved in four species of Odontomachus trap-jaw ants: male signals are more conserved, but are species specific. Bioassays implicate newly discovered compounds as fertility signals for O. ruginodis.

The Role of Anchor-Tipped Larval Hairs in the Organization of Ant Colonies

The spatial organization within a social insect colony is a key component of colony life. It influences individual interaction rates, resource distribution, and division of labor within the nest. Yet studies of social insect behavior are most often carried out in artificial constructions, which may change worker behavior and colony organization. We observed how workers of the ant Pheidole rhea organized brood in nests with deep chambers and textured walls that were designed to mimic their natural constructions more closely. Instead of clumping larvae into piles on the chamber floor, workers suspended fourth-instar larvae from the vertical walls and ceiling of each chamber while young larvae and pupae were clumped at the base. Fourth-instar larvae possess five rows of anchor-tipped hairs on their dorsal side, and we predicted that these hairs functioned to attach larvae to the nest walls. We gave larvae “haircuts,” where only the anchor-tipped hairs were removed, and then tested their ability to adhere to a textured surface raised to an angle of 90° and then 120° with respect to the horizontal plane. Larvae whose hairs had been clipped came unattached in almost all trials, while larvae whose hairs remained intact stayed attached. This confirmed that anchor-tipped hairs functioned to attach larvae to the walls of the nest. The presence of anchor-tipped hairs is widespread and has been documented in at least 22 genera from the ant subfamily Myrmicinae, including species that occur in a variety of environments and represent a broad range of nesting habits. Based on our results, it is likely that many species exhibit this larval hanging behavior, and this could impact colony characteristics such as spatial organization and the care of developing larvae by nurse workers.

Social insects inspire human design

The international conference ‘Social Biomimicry: Insect Societies and Human Design’, hosted by Arizona State University, USA, 18–20 February 2010, explored how the collective behaviour and nest architecture of social insects can inspire innovative and effective solutions to human design challenges. It brought together biologists, designers, engineers, computer scientists, architects and businesspeople, with the dual aims of enriching biology and advancing biomimetic design.

Army ants as research and collection tools.

Abstract Ants that fall prey to the raids of army ants commonly respond by evacuating their nests. This documented behavior has been underexploited by researchers as an efficient research tool. This study focuses on the evacuation response of the southwestern desert ant Aphaenogaster cockerelli André (Hymenoptera: Formicidae) to the army ant Newamyrmex nigrescens Cresson. It is shown that army ants can be used to collect mature colonies of ants. The applicability of this tool to ecologically meaningful areas of research is discussed.

Conserved male-specific cuticular hydrocarbon patterns in the trap-jaw ant Odontomachus brunneus

Cuticular hydrocarbons have been identified as the source of sex-recognition signals for many insects, but for social insects, specifically ants, cuticular hydrocarbon profiles of males are often ignored. This study reports male-specific cuticular hydrocarbon patterns for the trap-jaw ant Odontomachus brunneus. Analysis of samples from four Florida populations demonstrated that male-specific overabundance of four hydrocarbons is conserved across populations despite population-level divergence of the remainder of the profile. In addition, hydrocarbon patterns unique to adult males were not present on the cuticle of final instar male larvae, indicating that male-specific profiles arise late in development. The pattern of an abundant subset of conserved cuticular hydrocarbons characteristic of males across divergent populations was compared to earlier findings of the conservation of fertility signals of females across these same populations.