Pheromones and other kinds of chemical communication underlie the behavior of all animals Building on the strengths of the first edition, widely recognized as the leading text in the subject, this is a comprehensive overview of how pheromones work Extensively revised and expanded to cover advances made over the last ten years, the book offers a thorough exploration of the evolutionary and behavioral contexts of chemical communication along with a detailed introduction to the molecular and neural basis of signal perception through olfaction At a time of ever increasing specialization, Wyatt offers a unique synthesis, integrating examples across the animal kingdom A final chapter critically considers human pheromones and the importance of olfaction to human biology Its breadth of coverage and readability make the book an unrivaled resource for students and researchers in a range of fields from chemistry, genetics, genomics, molecular biology and neuroscience to ecology, evolution and behavior

Pheromones and Animal Behavior: Chemical Signals and Signatures

One of the conditions favoring the evolution and maintenance of sociality is the ability to discriminate between kin and non-kin, because it allows altruistic acts to be directed to recipients of high relatedness (Hamilton, 1987). Nestmate recognition is the process whereby social insects recognize individuals belonging to their own colony or an alien colony, and accordingly allow or prohibit entry to their nest. Nestmate recognition often results in the discrimination of kin from non-kin, but in social insects there is a distinction to be made between nestmate and kin recognition. Where kin recognition is the assessment of the degree of relatedness towards another individual, nestmate recognition is the binary recognition of group membership (Arnold et al. , 1996; Lenoir et al. , 1999). In ants, wasps and termites, the blend of hydrocarbons present on the cuticle appears to comprise the essential compounds that serve as nestmate recognition cues (Howard and Blomquist, 2005), although in honeybees fatty acids and esters may also play an important role (Breed, 1998a; but see Dani et al. , 2005; Ch?ine et al. , 2005). At the end of the 1990s, the notion that cuticular hydrocarbons act as recognition cues was supported mainly by correlative evidence (Singer, 1998; Vander Meer and Morel, 1998; Lenoir et al. , 1999), but significant progress has been made over the last decade.

Nestmate recognition in social insects and the role of hydrocarbons

Division of labour--individuals specializing in different activities--features prominently in the spectacular success of the social insects. Until recently, genetic and genomic analyses of division of labour were limited to just a few species. However, research on an ever-increasing number of species has provided new insight, from which we highlight two results. First, heritable influences on division of labour are more pervasive than previously imagined. Second, different forms of division of labour, in lineages in which eusociality has arisen independently, have evolved through changes in the regulation of highly conserved molecular pathways associated with several basic life-history traits, including nutrition, metabolism and reproduction.

Genetic and genomic analyses of the division of labour in insect societies

Although eusociality evolved independently within several orders of insects, research into the molecular underpinnings of the transition towards social complexity has been confined primarily to Hymenoptera (for example, ants and bees). Here we sequence the genome and stage-specific transcriptomes of the dampwood termite Zootermopsis nevadensis (Blattodea) and compare them with similar data for eusocial Hymenoptera, to better identify commonalities and differences in achieving this significant transition. We show an expansion of genes related to male fertility, with upregulated gene expression in male reproductive individuals reflecting the profound differences in mating biology relative to the Hymenoptera. For several chemoreceptor families, we show divergent numbers of genes, which may correspond to the more claustral lifestyle of these termites. We also show similarities in the number and expression of genes related to caste determination mechanisms. Finally, patterns of DNA methylation and alternative splicing support a hypothesized epigenetic regulation of caste differentiation.

/pdf/molecular-traces-of-alternative-social-organization-in-a-19xrmz0zyk.pdf

Molecular traces of alternative social organization in a termite genome

A major evolutionary transition to eusociality with reproductive division of labor between queens and workers has arisen independently at least 10 times in the ants, bees, and wasps. Pheromones produced by queens are thought to play a key role in regulating this complex social system, but their evolutionary history remains unknown. Here, we identify the first sterility-inducing queen pheromones in a wasp, bumblebee, and desert ant and synthesize existing data on compounds that characterize female fecundity in 64 species of social insects. Our results show that queen pheromones are strikingly conserved across at least three independent origins of eusociality, with wasps, ants, and some bees all appearing to use nonvolatile, saturated hydrocarbons to advertise fecundity and/or suppress worker reproduction. These results suggest that queen pheromones evolved from conserved signals of solitary ancestors.

https://science.sciencemag.org/content/sci/343/6168/287.full.pdf

Conserved class of queen pheromones stops social insect workers from reproducing.

A major transition in evolution is the origin of a division between reproduction and work among individuals. Nowhere is this divide more striking than in social insects, where workers rarely produce offspring even though they are often capable of reproduction should the queen or king die. The molecular mechanisms that control worker reproduction remain largely unknown. We used a combination of behavioral assays and RNA interference (RNAi) to identify a gene required for the reproductive division of labor between the queen and the workers.

https://zoo-kfoster.zoo.ox.ac.uk/sites/default/files/files/KorbetalScience2009.pdf

A Gene Necessary for Reproductive Suppression in Termites

Polyphenism, the expression of different phenotypes with the same genetic background, is well known for social insects. The substantial physiological and morphological differences among the castes generally are the result of differential gene expression. In lower termites, workers are developmentally flexible to become neotenic replacement reproductives via a single moult after the death of the founding reproductives. Thus, both castes (neotenics and workers) are expected to differ mainly in the expression of genes linked to reproductive division of labour, which constitutes the fundamental basis of insect societies. Representational difference analysis of cDNAs was used to study differential gene expression between neotenics and workers in the drywood termite Cryptotermes secundus (Kalotermitidae). We identified and, at least partially cloned five novel genes that were highly expressed in female neotenics. Quantitative real-time PCR analysis of all five genes in different castes (neotenics, founding reproductives, winged sexuals and workers of both sexes) confirmed the differential expression patterns. In addition, the relative expression of these genes was determined in three body parts of female neotenics (head, thorax, and abdomen) using quantitative real-time PCR. The identified genes could be involved in the control and regulation of reproductive division of labour. Interestingly, this study revealed an expression pattern partly similar to social Hymenoptera indicating both common and species-specific regulatory mechanisms in hemimetabolous and holometabolous social insects.

https://link.springer.com/content/pdf/10.1186%2F1471-2164-8-198.pdf

Molecular basis for the reproductive division of labour in a lower termite.

In social insects, it is assumed that signals of the queen inform nestmates about her reproductive status. Thus, workers forego their own reproduction if the queen signals high fertility. In hemimetabolous termites, little is known about reproductive inhibition, but evidence exists for a royal-pair control. Workers of lower termites exhibit a high developmental flexibility and are potentially able to become reproductives, but the presence of a fertile reproductive restrains them from reaching sexual maturity. The nature of this control, however, remains unknown. Here, we report on qualitative differences in cuticular hydrocarbon profiles between queens and workers of the basal drywood termite Cryptotermes secundus. Queens were characterized by a shift to long-chained and branched hydrocarbons. Most remarkably, similar chemical patterns are regarded as fertility cues of reproductives in social Hymenoptera. This might suggest that both groups of social insects convergently evolved similar chemical signatures. The present study provides deeper insights into how termites might have socially exploited these signatures from sexual communication in their cockroach-like ancestor.

Scent of a queen—cuticular hydrocarbons specific for female reproductives in lower termites

The molecular mechanisms regulating caste determination and reproductive division of labor, the hallmarks of insect societies, are poorly defined. The identification of key genes involved in these developmentally important processes will be essential to gain a better understanding of the mechanisms controlling one of the most impressive examples of polyphenism, the caste structure of eusocial species. Here, we applied representational difference analysis of cDNAs, to study differential gene expression between queens (female neotenics) and workers in the dry wood termite Cryptotermes cynocephalus and identified 13 genes that were highly expressed in queens. In addition, we partially cloned several homologous genes of the related termite species Cryptotermes secundus and compared the expression profiles of 10 homologous genes. In most cases, the preferential expression in female neotenics was not conserved between species, despite the close phylogenetic relationship of both Cryptotermes species. It is possible that these genes are associated with known species-specific differences in caste development modes. Only three genes (Neofem1, 2, and 3) showed a conserved and highly preferential expression in female neotenics, suggesting that their products may play important roles in female reproductives, in particular in controlling caste determination and reproductive division of labor.

Comparison of Queen-Specific Gene Expression in Related Lower Termite Species

The Caribbean island of Jamaica is home to a lineage of crabs (Crustacea: Decapoda: Brachyura: Sesarmidae) which have colonized the most unusual terrestrial habitats. Today, they can be found nesting in bromeliad leaf axils or empty snail shells, scurrying on the forest floor or among dry rock rubble, climbing on walls of deep cave systems, or digging burrows in the banks of mountain streams. In order to facilitate survival of their offspring in these remarkable and new habitats, complex behavioral adaptations have evolved, including feeding and protecting the offspring, and transport of empty snail shells into the nursery to buffer the pH and provide the necessary calcium carbonate [summarized in Diesel (Proc Roy Soc Lond B 264:1403–1406, 1997), Diesel and Schubart (Evolutionary ecology of social and sexual systems: crustaceans as model organisms. Oxford University Press, New York, pp 365–386, 2007)]. No other American sesarmid crab species shows this degree of terrestriality and elaborate brood care behavior. Instead, the most related species typically are inhabitants of marshes and mangroves and reproduce by releasing their larvae into the ocean, without any additional paternal obligation. Molecular phylogenetic analyses revealed that the Jamaican endemic sesarmids are monophyletic and thus the outcome of a single colonization event, which took place approximately 4.5 million years ago and was followed by a rapid radiation, speciation, and adaptation to ecological niches, which have not been used by crabs in any other parts of the world and required evolution of complex behavioral strategies to render survival in these habitats possible (Schubart et al. Nature 393:363–365, 1998a). This system can be considered a classic example of an adaptive radiation of comparatively young age. It calls for research concerning the mechanisms and the pace of evolution to generate these highly specialized forms. In the present paper, we provide new data on evolutionary processes at the intraspecific level, which may help to understand the potential of diversification in these crabs. Furthermore, published and unpublished data available for these specialized crabs are summarized, giving evidence for the astounding diversity of evolutionary strategies and the dimension of biodiversity beyond the species level.

/pdf/ongoing-phenotypic-and-genotypic-diversification-in-4utloa07b2.pdf

Tobias Weil

Papers

A Gene Necessary for Reproductive Suppression in Termites

Molecular basis for the reproductive division of labour in a lower termite.

Scent of a queen—cuticular hydrocarbons specific for female reproductives in lower termites

Comparison of Queen-Specific Gene Expression in Related Lower Termite Species

Ongoing Phenotypic and Genotypic Diversification in Adaptively Radiated Freshwater Crabs from Jamaica