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      Conserved Genes Underlie Phenotypic Plasticity in an Incipiently Social Bee

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          Abstract

          Despite a strong history of theoretical work on the mechanisms of social evolution, relatively little is known of the molecular genetic changes that accompany transitions from solitary to eusocial forms. Here, we provide the first genome of an incipiently social bee that shows both solitary and social colony organization in sympatry, the Australian carpenter bee Ceratina australensis. Through comparative analysis, we provide support for the role of conserved genes and cis-regulation of gene expression in the phenotypic plasticity observed in nest-sharing, a rudimentary form of sociality. Additionally, we find that these conserved genes are associated with caste differences in advanced eusocial species, suggesting these types of mechanisms could pave the molecular pathway from solitary to eusocial living. Genes associated with social nesting in this species show signatures of being deeply conserved, in contrast to previous studies in other bees showing novel and faster-evolving genes are associated with derived sociality. Our data provide support for the idea that the earliest social transitions are driven by changes in gene regulation of deeply conserved genes.

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          Most cited references53

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          The rapid evolution of reproductive proteins.

          Many genes that mediate sexual reproduction, such as those involved in gamete recognition, diverge rapidly, often as a result of adaptive evolution. This widespread phenomenon might have important consequences, such as the establishment of barriers to fertilization that might lead to speciation. Sequence comparisons and functional studies are beginning to show the extent to which the rapid divergence of reproductive proteins is involved in the speciation process.
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            Evolutionary changes in cis and trans gene regulation.

            Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.
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              Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

              The evolution of eusociality is one of the major transitions in evolution, but the underlying genomic changes are unknown. We compared the genomes of 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution, and report three major findings. First, many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Second, there is no single road map to eusociality; independent evolutionary transitions in sociality have independent genetic underpinnings. Third, though clearly independent in detail, these transitions do have similar general features, including an increase in constrained protein evolution accompanied by increases in the potential for gene regulation and decreases in diversity and abundance of transposable elements. Eusociality may arise through different mechanisms each time, but would likely always involve an increase in the complexity of gene networks.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                October 2018
                22 September 2018
                22 September 2018
                : 10
                : 10
                : 2749-2758
                Affiliations
                [1 ]Department of Biological Sciences, University of New Hampshire
                [2 ]Department of Cell & Developmental Biology, University of Pennsylvania
                [3 ]Department of Ecology, Evolution and Organismal Biology, Iowa State University
                [4 ]Department of Entomology, University of Georgia
                Author notes

                Sandra M. Rehan and Karl M. Glastad authors contributed equally to this work.

                Data deposition: Raw data have been submitted to the NCBI Sequence Read Archive (SRA) with accession number PRJNA302037.

                Corresponding author: E-mail: sandra.rehan@ 123456unh.edu .
                Author information
                http://orcid.org/0000-0002-6441-5155
                http://orcid.org/0000-0002-0030-9302
                Article
                evy212
                10.1093/gbe/evy212
                6190964
                30247544
                6e649a69-5569-4d88-9bb0-90c1ff4f0fe9
                © The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 19 September 2018
                Page count
                Pages: 10
                Funding
                Funded by: University of New Hampshire 10.13039/100008284
                Funded by: University of Georgia 10.13039/100007699
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: 1456283
                Award ID: 1456296
                Categories
                Research Article

                Genetics
                social transitions,phenotypic plasticity,molecular evolution,comparative genomics,taxonomically restricted genes,small carpenter bee

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