Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp,Polistes canadensis (original) (raw)
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Caste development and reproduction: a genome-wide analysis of hallmarks of insect eusociality
Insect Molecular Biology, 2006
The honey bee queen and worker castes are a model system for developmental plasticity. We used established expressed sequence tag information for a Gene Ontology based annotation of genes that are differentially expressed during caste development. Metabolic regulation emerged as a major theme, with a caste-specific difference in the expression of oxidoreductases vs. hydrolases. Motif searches in upstream regions revealed group-specific motifs, providing an entry point to cis-regulatory network studies on caste genes. For genes putatively involved in reproduction, meiosis-associated factors came out as highly conserved, whereas some determinants of embryonic axes either do not have clear orthologs (bag of marbles, gurken, torso), or appear to be lacking (trunk) in the bee genome. Our results are the outcome of a first genome-based initiative to provide an annotated framework for trends in gene regulation during female caste differentiation (representing developmental plasticity) and reproduction.
Gene expression and the evolution of phenotypic diversity in social wasps
BMC Biology, 2007
Background: Organisms are capable of developing different phenotypes by altering the genes they express. This phenotypic plasticity provides a means for species to respond effectively to environmental conditions. One of the most dramatic examples of phenotypic plasticity occurs in the highly social hymenopteran insects (ants, social bees, and social wasps), where distinct castes and sexes all arise from the same genes. To elucidate how variation in patterns of gene expression affects phenotypic variation, we conducted a study to simultaneously address the influence of developmental stage, sex, and caste on patterns of gene expression in Vespula wasps. Furthermore, we compared the patterns found in this species to those found in other taxa in order to investigate how variation in gene expression leads to phenotypic evolution.
A molecular concept of caste in insect societies
Current opinion in insect science, 2018
The term 'caste' is used to describe the division of reproductive labour that defines eusocial insect societies. The definition of 'caste' has been debated over the last 50 years, specifically with respect to the simplest insect societies; this raises the question of whether a simple categorisation of social behaviour by reproductive state alone is helpful. Gene-level analyses of behaviours of individuals in hymenopteran social insect societies now provide a new empirical base-line for defining caste and understanding the evolution and maintenance of a reproductive division of labour. We review this literature to identify a set of potential molecular signatures that, combined with behavioural, morphological and physiological data, help define caste more precisely; these signatures vary with the type of society, and are likely to be influenced by ecology, life-history, and stage in the colony cycle. We conclude that genomic approaches provide us with additional ways t...
Developmental regulation of caste-specific characters in social-insect polyphenism
Evolution and Development, 2005
Phenotypes of organisms are not determined completely genetically, but vary according to environmental factors (phenotypic plasticity). Some organisms express several discrete adaptive phenotypes (polyphenism). Social insects possess a few types of individuals (castes) in their colonies, to which specific tasks are allocated. Here, I review studies on caste polyphenism in ants and termites, in terms of the developmental mechanisms of caste-specific characters, such as alate wings and soldier mandibles. In ants, the developmental fate of caste is probably determined by the pattern-formation genes in the early stage of postembryonic development, but apoptotic degeneration occurs in the wing primordia of future workers. As apoptotic wing degeneration has been observed in two phylogenetically distant groups of ants, this phenomenon is suggested to be conserved in many ant species. On the other hand, all termite species possess distinct sterile soldiers with specific morphologies suitable for defense. Recent studies using molecular techniques isolated genes related to soldier differentiation and analyzed the expression profiles of those genes in order to understand the mechanism of caste differentiation and the link between molecular and social evolution. In this review, I focus on these studies, in terms of the alteration of body plan in response to environmental signals, and discuss the evolutionary process of the interaction between ontogeny and environment.
Proximate mechanisms and evolution of caste polyphenism in social insects: From sociality to genes
Ecological Research, 2004
Evidence has accumulated over several decades to prove the kin selection theory of evolution of social insects, however, proximate mechanisms of social behavior, and/or caste differentiation remain obscure. Genes that regulate these mechanisms are apparently selected through kin selection, and organisms have consequently acquired sociality. Here, I will discuss several studies that were performed recently by Matsumoto Laboratory, University of Tokyo, Tokyo, Japan, in various social insects, such as termites and ants, in order to reveal the regulatory mechanisms of social behavior and the evolutionary processes of sociality. First, I will review the foraging behavior of the black marching termite Hospitalitermes medioflavus, where well-organized task allocation among castes is apparent. This suggests that regulation of postembryonic development is important in social behavior. Next, I will summarize recent progress in identifying caste-specific gene expression in the damp-wood termite Hodotermopsis sjostedti. This constitutes the basis for molecular mechanisms of caste differentiation, and moreover, the genes identified might be good markers for social evolution. Finally, the mechanism underlying winglessness in ant workers is reviewed. Apoptotic cell death was detected at the stage of pupation in wingless worker castes. Furthermore, the areas of study recently designated as 'sociogenomics' and 'ecological developmental biology' are discussed.
Proceedings of the National Academy of Sciences, 2007
Colonies of social wasps, ants, and bees are characterized by the production of two phenotypes of female offspring, workers that remain at their natal nest and nonworkers that are potential colony reproductives of the next generation. The phenotype difference includes morphology and is fixed during larval development in ants, honey bees, and some social wasps, all of which represent an advanced state of sociality. Paper wasps (Polistes) lack morphological castes and are thought to more closely resemble an ancestral state of sociality wherein the phenotype difference between workers and nonworkers is established only during adult life. We address an alternative hypothesis: a bias toward the potential reproductive (gyne) phenotype among Polistes female offspring occurs during larval development and is based on a facultatively expressed ancestral life history trait: diapause. We show that two signatures of diapause (extended maturation time and enhanced synthesis and sequestration of a hexameric storage protein) characterize the development of gyne offspring in Polistes metricus. Hexameric storage proteins are implicated in silencing juvenile hormone signaling, which is a prerequisite for diapause. Diverging hexamerin protein dynamics driven by changes in larval provisioning levels thereby provide one possible mechanism that can cause an adaptive shift in phenotype bias during the Polistes colony cycle. This ontogenetic basis for alternative female phenotypes in Polistes challenges the view that workers and gynes represent behavior options equally available to every female offspring, and it exemplifies how social insect castes can evolve from casteless lineages.
Molecular Ecology, 2014
Variation in gene expression leads to phenotypic diversity and plays a central role in caste differentiation of eusocial insect species. In social Hymenoptera, females with the same genetic background can develop into queens or workers, which are characterized by divergent morphologies, behaviours and lifespan. Moreover, many social insects exhibit behaviourally distinct worker castes, such as brood-tenders and foragers. Researchers have just started to explore which genes are differentially expressed to achieve this remarkable phenotypic plasticity. Although the queen is normally the only reproductive individual in the nest, following her removal, young brood-tending workers often develop ovaries and start to reproduce. Here, we make use of this ability in the ant Temnothorax longispinosus and compare gene expression patterns in the queens and three worker castes along a reproductive gradient. We found the largest expression differences between the queen and the worker castes (~2500 genes) and the smallest differences between infertile brood-tenders and foragers (~300 genes). The expression profile of fertile workers is more worker-like, but to a certain extent intermediate between the queen and the infertile worker castes. In contrast to the queen, a high number of differentially expressed genes in the worker castes are of unknown function, pointing to the derived status of hymenopteran workers within insects.
The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolu- tion. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subse- quently studied the relative rates of molecular evolution at these caste-associ- ated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associ- ated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste.
Taxonomically restricted genes are associated with the evolution of sociality in the honey bee
Background: Studies have shown that taxonomically restricted genes are significant in number and important for the evolution of lineage specific traits. Social insects have gained many novel morphological and behavioral traits relative to their solitary ancestors. The task repertoire of an advanced social insect, for example, can be 40-50 tasks, about twice that of a solitary wasp or bee. The genetic basis of this expansion in behavioral repertoire is still poorly understood, and a role for taxonomically restricted genes has not been explored at the whole genome level. Results: Here we present comparative genomics results suggesting that taxonomically restricted genes may have played an important role in generating the expansion of behavioral repertoire associated with the evolution of eusociality. First, we show that the current honey bee official gene set contains about 700 taxonomically restricted genes. These are split between orphans, genes found only in the Hymenoptera, and genes found only in insects. Few of the orphans or genes restricted to the Hymenoptera have been the focus of experimental work, but several of those that have are associated with novel eusocial traits or traits thought to have changed radically as a consequence of eusociality. Second, we predicted that if taxonomically restricted genes are important for generating novel eusocial traits, then they should be expressed with greater frequency in workers relative to the queen, as the workers exhibit most of the novel behavior of the honey bee relative to their solitary ancestors. We found support for this prediction. Twice as many taxonomically restricted genes were found amongst the genes with higher expression in workers compared to those with higher expression in queens. Finally, we compiled an extensive list of candidate taxonomically restricted genes involved in eusocial evolution by analyzing several caste specific gene expression data sets. Conclusions: This work identifies a large number of candidate taxonomically restricted genes that may have played a role in eusocial evolution. This work thus lays the foundation for future functional genomics work on the evolution of novelty in the context of social behavior. We also present preliminary evidence, based on biased patterns of gene expression, that taxonomically restricted genes may have played a role in the evolution of caste systems, a characteristic lineage specific social trait.
Developmental Evolution in Social Insects: Regulatory Networks from Genes to Societies
Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 2012
The evolution and development of complex phenotypes in social insect colonies, such as queenworker dimorphism or division of labor, can, in our opinion, only be fully understood within an expanded mechanistic framework of Developmental Evolution. Conversely, social insects offer a fertile research area in which fundamental questions of Developmental Evolution can be addressed empirically. We review the concept of gene regulatory networks (GRNs) that aims to fully describe the battery of interacting genomic modules that are differentially expressed during the development of individual organisms. We discuss how distinct types of network models have been used to study different levels of biological organization in social insects, from GRNs to social networks. We propose that these hierarchical networks spanning different organizational levels from genes to societies should be integrated and incorporated into full GRN models to elucidate the evolutionary and developmental mechanisms underlying social insect phenotypes. Finally, we discuss prospects and approaches to achieve such an integration. How to cite this article: Linksvayer TA, Fewell JH, Gadau J, Laubichler MD. 2011. Developmental evolution in social insects: regulatory networks from genes to societies. J. Exp. Zool. (Mol. Dev. Evol.) 318:159-169.