Chemical Ecology and Sociality in Aphids: Opportunities and Directions.

Aphids have long been recognized as good phytochemists. They are small sap-feeding plant herbivores with complex life cycles that can involve cyclical parthenogenesis and seasonal host plant alternation, and most are plant specialists. Aphids have distinctive traits for identifying and exploiting their host plants, including the expression of polyphenisms, a form of discrete phenotypic plasticity characteristic of insects, but taken to extreme in aphids. In a relatively small number of species, a social polyphenism occurs, involving sub-adult "soldiers" that are behaviorally or morphologically specialized to defend their nestmates from predators. Soldiers are sterile in many species, constituting a form of eusociality and reproductive division of labor that bears striking resemblances with other social insects. Despite a wealth of knowledge about the chemical ecology of non-social aphids and their phytophagous lifestyles, the molecular and chemoecological mechanisms involved in social polyphenisms in aphids are poorly understood. We provide a brief primer on aspects of aphid life cycles and chemical ecology for the non-specialists, and an overview of the social biology of aphids, with special attention to chemoecological perspectives. We discuss some of our own efforts to characterize how host plant chemistry may shape social traits in aphids. As good phytochemists, social aphids provide a bridge between the study of insect social evolution sociality, and the chemical ecology of plant-insect interactions. Aphids provide many promising opportunities for the study of sociality in insects, and to understand both the convergent and novel traits that characterize complex sociality on plants.

Effects of nutritional deprivation on development and behavior in the subsocial bee Ceratina calcarata (Hymenoptera: Xylocopinae).

By manipulating resources or dispersal opportunities, mothers can force offspring to remain at the nest to help raise siblings, creating a division of labor. In the subsocial bee Ceratina calcarata, mothers manipulate the quantity and quality of pollen provided to the first female offspring, producing a dwarf eldest daughter that is physically smaller and behaviorally subordinate. This daughter forages for her siblings and forgoes her own reproduction. To understand how the mother's manipulation of pollen affects the physiology and behavior of her offspring, we manipulated the amount of pollen provided to offspring and measured the effects of pollen quantity on offspring development, adult body size and behavior. We found that by experimentally manipulating pollen quantities we could recreate the dwarf eldest daughter phenotype, demonstrating how nutrient deficiency alone can lead to the development of a worker-like daughter. Specifically, by reducing the pollen and nutrition to offspring, we significantly reduced adult body size and lipid stores, creating significantly less aggressive, subordinate individuals. Worker behavior in an otherwise solitary bee begins to explain how maternal manipulation of resources could lead to the development of social organization and reproductive hierarchies, a major step in the transition to highly social behaviors.

An alternative pathway to eusociality: Exploring the molecular and functional basis of fortress defense.

Some animals express a form of eusociality known as "fortress defense," in which defense rather than brood care is the primary social act. Aphids are small plant-feeding insects, but like termites, some species express division of labor and castes of aggressive juvenile "soldiers." What is the functional basis of fortress defense eusociality in aphids? Previous work showed that the acquisition of venoms might be a key innovation in aphid social evolution. We show that the lethality of aphid soldiers derives in part from the induction of exaggerated immune responses in insects they attack. Comparisons between closely related social and nonsocial species identified a number of secreted effector molecules that are candidates for immune modulation, including a convergently recruited protease described in unrelated aphid species with venom-like functions. These results suggest that aphids are capable of antagonizing conserved features of the insect immune response, and provide new insights into the mechanisms underlying the evolution of fortress defense eusociality in aphids.

The Genome and Methylome of a Subsocial Small Carpenter Bee, Ceratina calcarata.

Understanding the evolution of animal societies, considered to be a major transition in evolution, is a key topic in evolutionary biology. Recently, new gateways for understanding social evolution have opened up due to advances in genomics, allowing for unprecedented opportunities in studying social behavior on a molecular level. In particular, highly eusocial insect species (caste-containing societies with nonreproductives that care for siblings) have taken center stage in studies of the molecular evolution of sociality. Despite advances in genomic studies of both solitary and eusocial insects, we still lack genomic resources for early insect societies. To study the genetic basis of social traits requires comparison of genomes from a diversity of organisms ranging from solitary to complex social forms. Here we present the genome of a subsocial bee, Ceratina calcarata This study begins to address the types of genomic changes associated with the earliest origins of simple sociality using the small carpenter bee. Genes associated with lipid transport and DNA recombination have undergone positive selection in C. calcarata relative to other bee lineages. Furthermore, we provide the first methylome of a noneusocial bee. Ceratina calcarata contains the complete enzymatic toolkit for DNA methylation. As in the honey bee and many other holometabolous insects, DNA methylation is targeted to exons. The addition of this genome allows for new lines of research into the genetic and epigenetic precursors to complex social behaviors.

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus.

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum-likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host-associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall-forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host-plant-associated differentiation were greater in the non-gall-inducing parasites than in their gall-inducing hosts. RNA-seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host-plant relationships. Our results suggest a mode of speciation in which host plants drive within-guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.