Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees

While it is well known that the genome can affect social behavior, recent models posit that social lifestyles can, in turn, influence genome evolution. Here, we perform the most phylogenetically comprehensive comparative analysis of 16 bee genomes to date: incorporating two published and four new carpenter bee genomes (Apidae: Xylocopinae) for a first-ever genomic comparison with a monophyletic clade containing solitary through advanced eusocial taxa. We find that eusocial lineages have undergone more gene family expansions, feature more signatures of positive selection, and have higher counts of taxonomically restricted genes than solitary and weakly social lineages. Transcriptomic data reveal that caste-affiliated genes are deeply-conserved; gene regulatory and functional elements are more closely tied to social phenotype than phylogenetic lineage; and regulatory complexity increases steadily with social complexity. Overall, our study provides robust empirical evidence that social evolution can act as a major and surprisingly consistent driver of macroevolutionary genomic change.

Synteny-based analyses indicate that sequence divergence is not the main source of orphan genes

The origin of ‘orphan’ genes, species-specific sequences that lack detectable homologues, has remained mysterious since the dawn of the genomic era. There are two dominant explanations for orphan genes: complete sequence divergence from ancestral genes, such that homologues are not readily detectable; and de novo emergence from ancestral non-genic sequences, such that homologues genuinely do not exist. The relative contribution of the two processes remains unknown. Here, we harness the special circumstance of conserved synteny to estimate the contribution of complete divergence to the pool of orphan genes. By separately comparing yeast, fly and human genes to related taxa using conservative criteria, we find that complete divergence accounts, on average, for at most a third of eukaryotic orphan and taxonomically restricted genes. We observe that complete divergence occurs at a stable rate within a phylum but at different rates between phyla, and is frequently associated with gene shortening akin to pseudogenization.

New Non-Bilaterian Transcriptomes Provide Novel Insights into the Evolution of Coral Skeletomes

A general trend observed in animal skeletomes—the proteins occluded in animal skeletons—is the copresence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend. However, distributions and phylogenetic analyses of biomineralization-related genes are often based on only a few species, with other anthozoan calcifiers such as octocorals (soft corals), not being fully considered. We de novo assembled the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published nonbilaterian transcriptome resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. Cnidaria shared no skeletome proteins with Placozoa or Ctenophora, but did share some skeletome proteins with Porifera, such as galaxin-related proteins. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes such as secreted acidic proteins, scleritin, and carbonic anhydrases, and propose an early, single biomineralization-recruitment event for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia–Scleractinia transition, but appears to be associated with protein secretion into the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e., aragonite/calcite) with no differences in the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins such as galaxins and SCRiP-3a could represent instances of commonality.

Synteny-based analyses indicate that sequence divergence is not the main source of orphan genes

The origin of “orphan” genes, species-specific sequences that lack detectable homologues, has remained mysterious since the dawn of the genomic era. There are two dominant explanations for orphan genes: complete sequence divergence from ancestral genes, such that homologues are not readily detectable; and de novo emergence from ancestral non-genic sequences, such that homologues genuinely do not exist. The relative contribution of the two processes remains unknown. Here, we harness the special circumstance of conserved synteny to estimate the contribution of complete divergence to the pool of orphan genes. By separately comparing yeast, fly and human genes to related taxa using conservative criteria, we find that complete divergence accounts, on average, for at most a third of eukaryotic orphan and taxonomically restricted genes. We observe that complete divergence occurs at a stable rate within a phylum but at different rates between phyla, and is frequently associated with gene shortening akin to pseudogenization. Two cancer-related human genes, DEC1 and DIRC1, have likely originated via this route in a primate ancestor.

New non-bilaterian transcriptomes provide novel insights into the evolution of coral skeletomes

A general feature of animal skeletomes is the co-presence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend, however in this group distribution and phylogenetic analyses of biomineralization-related genes have been often based on limited numbers of species, with other anthozoan calcifiers such as octocorals, being overlooked. We de-novo sequenced the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published non-bilaterian transcriptomic resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. At the large scale, no protein showed a ‘Cnidaria+Placozoa’ or ‘Cnidaria+Ctenophora’ distribution, while some were found in cnidarians and Porifera. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes (TRGs) and propose an alternative evolutionary scenario, involving an early single biomineralization-recruitment event, for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia-Scleractinia transition, but appears to be associated with protein secretion in the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e. aragonite/calcite) with no differences on the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins like galaxins and SCRiP-3a could represent instances of commonality.

The genome of Aiptasia, a sea anemone model for coral symbiosis

The most diverse marine ecosystems, coral reefs, depend upon a functional symbiosis between a cnidarian animal host (the coral) and intracellular photosynthetic dinoflagellate algae. The molecular and cellular mechanisms underlying this endosymbiosis are not well understood, in part because of the difficulties of experimental work with corals. The small sea anemone Aiptasia provides a tractable laboratory model for investigating these mechanisms. Here we report on the assembly and analysis of the Aiptasia genome, which will provide a foundation for future studies and has revealed several features that may be key to understanding the evolution and function of the endosymbiosis. These features include genomic rearrangements and taxonomically restricted genes that may be functionally related to the symbiosis, aspects of host dependence on alga-derived nutrients, a novel and expanded cnidarian-specific family of putative pattern-recognition receptors that might be involved in the animal–algal interactions, and extensive lineage-specific horizontal gene transfer. Extensive integration of genes of prokaryotic origin, including genes for antimicrobial peptides, presumably reflects an intimate association of the animal–algal pair also with its prokaryotic microbiome.