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.
The mushroom bodies are regions in the insect brain involved in processing complex multimodal information. They are composed of many parallel sets of intrinsic neurons that receive input from and transfer output to extrinsic neurons that connect the mushroom bodies with the surrounding neuropils. Mushroom bodies are particularly large in social Hymenoptera and are thought to be involved in the control of conspicuous orientation, learning, and memory capabilities of these insects. The present account compares the organization of sensory input to the mushroom body's calyx in different Hymenoptera. Tracer and conventional neuronal staining procedures reveal the following anatomic characteristics: The calyx comprises three subdivisions, the lip, collar, and basal ring. The lip receives antennal lobe afferents, and these olfactory input neurons can terminate in two or more segregated zones within the lip. The collar receives visual afferents that are bilateral with equal representation of both eyes in each calyx. Visual inputs provide two to three layers of processes in the collar subdivision. The basal ring is subdivided into two modality-specific zones, one receiving visual, the other antennal lobe input. Some overlap of modality exists between calycal subdivisions and within the basal ring, and the degree of segregation of sensory input within the calyx is species-specific. The data suggest that the many parallel channels of intrinsic neurons may each process different aspects of sensory input information.
We report the draft genome sequence of the red harvester ant, Pogonomyrmex barbatus. The genome was sequenced using 454 pyrosequencing, and the current assembly and annotation were completed in less than 1 y. Analyses of conserved gene groups (more than 1,200 manually annotated genes to date) suggest a high-quality assembly and annotation comparable to recently sequenced insect genomes using Sanger sequencing. The red harvester ant is a model for studying reproductive division of labor, phenotypic plasticity, and sociogenomics. Although the genome of P. barbatus is similar to other sequenced hymenopterans (Apis mellifera and Nasonia vitripennis) in GC content and compositional organization, and possesses a complete CpG methylation toolkit, its predicted genomic CpG content differs markedly from the other hymenopterans. Gene networks involved in generating key differences between the queen and worker castes (e.g., wings and ovaries) show signatures of increased methylation and suggest that ants and bees may have independently co-opted the same gene regulatory mechanisms for reproductive division of labor. Gene family expansions (e.g., 344 functional odorant receptors) and pseudogene accumulation in chemoreception and P450 genes compared with A. mellifera and N. vitripennis are consistent with major life-history changes during the adaptive radiation of Pogonomyrmex spp., perhaps in parallel with the development of the North American deserts.T he formation of higher-level organization from independently functioning elements has resulted in some of the most significant transitions in biological evolution (1). These include the transition from prokaryotes to eukaryotes and from uni-to multicellular organisms, as well as the formation of complex animal societies with sophisticated division of labor among individuals. In eusocial insects such as ants, distinct morphological castes specialize in either reproduction or labor (2). Currently, very little is known of the genetic basis of caste and reproductive division of labor in these societies, where individuals follow different developmental trajectories, much like distinct cell lines in an organism (3). The resulting phenotypes, queens and workers, can differ greatly in morphology, physiology, and behavior, as well as in order of magnitude differences in life span and reproductive potential (2). Ants, of all social insects, arguably exhibit the highest diversity in social complexity, such as queen number, mating frequency, and the degree of complexity of division of labor (2), and most social traits have independent origins within the ants, making them well suited to comparative genomic analyses.The sequencing of the honey bee (Apis mellifera) genome marked a milestone in sociogenomics (4, 5), facilitating research on the evolution and maintenance of sociality from its molecular building blocks. Since then, genomes of three closely related species of solitary parasitic hymenopterans, Nasonia spp., were published and similarities and differences were extensively discuss...
Insect mushroom bodies are brain regions that receive multisensory input and are thought to play an important role in learning and memory. In most neopteran insects, the mushroom bodies receive direct olfactory input. In addition, the calyces of Hymenoptera receive substantial direct input from the optic lobes. We describe visual inputs to the calyces of the mushroom bodies of the honeybee Apis mellifera, the neurons' dendritic fields in the optic lobes, the medulla and lobula, and the organization of their terminals in the calyces. Medulla neurons terminate in the collar region of the calyx, where they segregate into five layers that receive alternating input from the dorsal or ventral medulla, respectively. A sixth, innermost layer of the collar receives input from lobula neurons. In the basal ring region of the calyx, medulla neuron terminals are restricted to a small, distal part. Lobula neurons are more prominent in the basal ring, where they terminate in its outer half. Although the collar and basal ring layers generally receive segregated input from both optic neuropils, some overlap occurs at the borders of the layers. At least three different types of mushroom body input neurons originate from the medulla: (a) neurons with narrow dendritic fields mainly restricted to the vicinity of the medulla's serpentine layer and found throughout the medulla; (b) neurons restricted to the ventral half of the medulla and featuring long columnar dendritic branches in the outer medulla; and (c) a group of neurons whose dendrites are restricted to the most ventral part of the medulla and whose axons form the anterior inferior optic tract. Most medulla neurons (groups a and b) send their axons via the anterior superior optic tract to the mushroom bodies. Neurons connecting the lobula with the mushroom bodies have their dendrites in a defined dorsal part of the lobula. Their axons form a third tract to the mushroom bodies, here referred to as the lobula tract. Our findings match the anatomy of intrinsic mushroom body neurons (Strausfeld, 2002) and together indicate that the mushroom bodies may be composed of many more functional subsystems than previously suggested.
Animals use vision to perform such diverse behaviors as finding food, interacting socially with other animals, choosing a mate, and avoiding predators. These behaviors are complex and the visual system must process color, motion, and pattern cues efficiently so that animals can respond to relevant stimuli. The visual system achieves this by dividing visual information into separate pathways, but to what extent are these parallel streams separated in the brain? To answer this question, we recorded intracellularly in vivo from 105 morphologically identified neurons in the lobula, a major visual processing structure of bumblebees (Bombus impatiens). We found that these cells have anatomically segregated dendritic inputs confined to one or two of six lobula layers. Lobula neurons exhibit physiological characteristics common to their respective input layer. Cells with arborizations in layers 1-4 are generally indifferent to color but sensitive to motion, whereas layer 5-6 neurons often respond to both color and motion cues. Furthermore, the temporal characteristics of these responses differ systematically with dendritic branching pattern. Some layers are more temporally precise, whereas others are less precise but more reliable across trials. Because different layers send projections to different regions of the central brain, we hypothesize that the anatomical layers of the lobula are the structural basis for the segregation of visual information into color, motion, and stimulus timing.
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