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Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

ABSTRACT: 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.

SUBMITTER: Kapheim KM

PROVIDER: S-EPMC5471836 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

Kapheim Karen M KM Pan Hailin H Li Cai C Salzberg Steven L SL Puiu Daniela D Magoc Tanja T Robertson Hugh M HM Hudson Matthew E ME Venkat Aarti A Fischman Brielle J BJ Hernandez Alvaro A Yandell Mark M Ence Daniel D Holt Carson C Yocum George D GD Kemp William P WP Bosch Jordi J Waterhouse Robert M RM Zdobnov Evgeny M EM Stolle Eckart E Kraus F Bernhard FB Helbing Sophie S Moritz Robin F A RF Glastad Karl M KM Hunt Brendan G BG Goodisman Michael A D MA Hauser Frank F Grimmelikhuijzen Cornelis J P CJ Pinheiro Daniel Guariz DG Nunes Francis Morais Franco FM Soares Michelle Prioli Miranda MP Tanaka Érica Donato ÉD Simões Zilá Luz Paulino ZL Hartfelder Klaus K Evans Jay D JD Barribeau Seth M SM Johnson Reed M RM Massey Jonathan H JH Southey Bruce R BR Hasselmann Martin M Hamacher Daniel D Biewer Matthias M Kent Clement F CF Zayed Amro A Blatti Charles C Sinha Saurabh S Johnston J Spencer JS Hanrahan Shawn J SJ Kocher Sarah D SD Wang Jun J Wang Jun J Robinson Gene E GE Zhang Guojie G

Science (New York, N.Y.) 20150514 6239

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 evo ...[more]

PMID: 25977371

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Project description:Coleoid cephalopods show unique morphological and neural novelties, such as arms with tactile and chemosensory suckers and a large complex nervous system. The evolution of such cephalopod novelties has been attributed at a genomic level to independent gene family expansions, yet the exact association and the evolutionary timing remain unclear. In the octopus genome, one such expansion occurred in the G-protein-coupled receptors (GPCRs) repertoire, a superfamily of proteins that mediate signal transduction. Here, we assessed the evolutionary history of this expansion and its relationship with cephalopod novelties. Using phylogenetic analyses, at least two cephalopod- and two octopus-specific GPCR expansions were identified. Signatures of positive selection were analysed within the four groups, and the locations of these sequences in the Octopus bimaculoides genome were inspected. Additionally, the expression profiles of cephalopod GPCRs across various tissues were extracted from available transcriptomic data. Our results reveal the evolutionary history of cephalopod GPCRs. Unexpanded cephalopod GPCRs shared with other bilaterians were found to be mainly nervous tissue specific. By contrast, duplications that are shared between octopus and the bobtail squid or specific to the octopus' lineage generated copies with divergent expression patterns devoted to tissues outside of the brain. The acquisition of novel expression domains was accompanied by gene order rearrangement through either translocation or duplication and gene loss. Lastly, expansions showed signs of positive selection and some were found to form tandem clusters with shared conserved expression profiles in cephalopod innovations such as the axial nerve cord. Altogether, our results contribute to the understanding of the molecular and evolutionary history of signal transduction and provide insights into the role of this expansion during the emergence of cephalopod novelties and/or adaptations.

Dataset Information

Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

Publications

Social evolution. Genomic signatures of evolutionary transitions from solitary to group living.

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