Genomic signatures of evolutionary transitions from solitary to group living

Kapheim, Karen M.; Pan, Hailin; Cai, Li; Salzberg, Steven L.; Puiu, Daniela; Magoč, Tanja; Robertson, Hugh M.; Hudson, Matthew E.; Venkat, Aarti; Fischman, Brielle J.; Hernández, Álvaro Gonzalez; Yandell, Mark; Ence, Daniel; Holt, Carson; Yocum, George D.; Kemp, William P.; Bosch, Jordi; Waterhouse, Robert M.; Zdobnov, Evgeny M.; Stolle, Eckart; Kraus, Frank Bernhard; Helbing, Sophie; Moritz, Robin F. A.; Glastad, Karl M.; Hunt, Brendan G.; Goodisman, Michael A. D.; Hauser, Frank; Grimmelikhuijzen, Cornelis J.P.; Pinheiro, Daniel Guariz; Nunes, Francis Morais Franco; Soares, Michelle P rioli Miranda; Tanaka, Erica D.; Simões, Zilá Luz Paulino; Hartfelder, Klaus; Evans, Jay D.; Barribeau, Seth M.; Johnson, Reed M.; Massey, Jonathan H.; Southey, Bruce R.; Hasselmann, Martin; Hamacher, Daniel; Biewer, Matthias; Kent, Clement F.; Zayed, Amro; Blatti, Charles; Sinha, Saurabh; Johnston, J. Spencer; Hanrahan, Shawn J.; Kocher, Sarah D.; Wang, Jun; Robinson, Gene E.; Zhang, Guojie

doi:10.1126/science.aaa4788

Cited by 359 publications

(525 citation statements)

References 144 publications

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“…1D and SI Text, section II.7). Transposable elements were recently identified as potentially important in the evolution of social complexity in bees (6). quadriceps.…”

Section: Resultsmentioning

confidence: 99%

“…The profound action of evolution in the generation of biological diversity can be discerned from the genome (6). However, genome sequence alone is not sufficient to explain diverse phenotypic variation because such analyses infer associations based on gene evolution and gene sharing rather than directly identifying differentially expressed genes (DEGs) in the phenotypes of interest (7).…”

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confidence: 99%

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Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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“…1D and SI Text, section II.7). Transposable elements were recently identified as potentially important in the evolution of social complexity in bees (6). quadriceps.…”

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

278

View full text Add to dashboard Cite

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“…dorsata seems likely. The frequent and independent duplication of fem in Hymenopteran lineages (Geuverink and Beukeboom, 2014;Koch et al, 2014) (Bee10Genome consortium, Kapheim et al, 2015) seems to be a general phenomenon, which may be of broader relevance to better understand the evolution of sex determination pathways in other insect species.…”

Section: Discussionmentioning

confidence: 99%

Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea

2015

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Studying the fate of duplicated genes provides informative insight into the evolutionary plasticity of biological pathways to which they belong. In the paralogous sex-determining genes complementary sex determiner (csd) and feminizer (fem) of honey bee species (genus Apis), only heterozygous csd initiates female development. Here, the full-length coding sequences of the genes csd and fem of the phylogenetically basal dwarf honey bee Apis florea are characterized. Compared with other Apis species, remarkable evolutionary changes in the formation and localization of a protein-interacting (coiled-coil) motif and in the amino acids coding for the csd characteristic hypervariable region (HVR) are observed. Furthermore, functionally different csd alleles were isolated as genomic fragments from a random population sample. In the predicted potential specifying domain (PSD), a high ratio of π N /π S = 1.6 indicated positive selection, whereas signs of balancing selection, commonly found in other Apis species, are missing. Low nucleotide diversity on synonymous and genome-wide, non-coding sites as well as site frequency analyses indicated a strong impact of genetic drift in A. florea, likely linked to its biology. Along the evolutionary trajectory of 30 million years of csd evolution, episodic diversifying selection seems to have acted differently among distinct Apis branches. Consistently low amino-acid differences within the PSD among pairs of functional heterozygous csd alleles indicate that the HVR is the most important region for determining allele specificity. We propose that in the early history of the lineage-specific fem duplication giving rise to csd in Apis, A. florea csd stands as a remarkable example for the plasticity of initial sex-determining signals.

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“…The phylogeny of bees based on AKHRs was consistent with their social complexity (Kapheim et al, 2015), which might imply that there were some differences contributing to the eusocial evolution since the evolutionary distances were computed based on the units of the number of amino acid substitutions per site (Tamura et al, 2013). However, the sequence alignment results demonstrated that AKHRs of bees shared an overall common sequence similarity besides the motifs discussed above, but less conserved N-termini, in which no relevance of eusocial evolution had been detected.…”

Section: Discussionmentioning

confidence: 56%

“…The eusocial evolution is associated with an increased capacity for gene regulation and a relaxed natural selection. As the "core set", AKH and AKHR were identified in all bee species (Kapheim et al, 2015). The mature AKH has been identified via mass spectrometry in the solitary bees (Lorenz et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

Prediction of the post-translational modifications of adipokinetic hormone receptors from solitary to eusocial bees

et al. 2018

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Adipokinetic hormone receptor (AKHR) was regarded as the crucial regulator of lipid consuming, but now has been renewed as a pluripotent neuropeptide G protein-coupled receptor. It has been identified in all sequenced bee genomes from the solitary to the eusocial. In the current study, we try to clarify the transitions of AKHR on lipid utilization and other potential functions from solitary to eusocial bees. The results showed that the AKHRs were divided into different groups based on their social complexity approximately. Nevertheless, the critical motifs and tertiary structures were highly conserved. As to the post-translational modifications, the eusocial possessed more phosphorylation residues and modification patterns, which might be due to the necessity of more diverse functions. These results suggest that AKHRs are highly conserved on both primary motifs and tertiary structures, but more flexible on posttranslational modifications so as to accommodate to more complicated eusocial life.

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Genomic signatures of evolutionary transitions from solitary to group living

Cited by 359 publications

References 144 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea

Prediction of the post-translational modifications of adipokinetic hormone receptors from solitary to eusocial bees

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