Abstract
Reconstructing the genomes of bilaterian ancestors is central to our understanding of animal evolution, where knowledge from ancient and/or slow-evolving bilaterian lineages is critical. Here we report a high-quality, chromosome-anchored reference genome for the scallop Patinopecten yessoensis, a bivalve mollusc that has a slow-evolving genome with many ancestral features. Chromosome-based macrosynteny analysis reveals a striking correspondence between the 19 scallop chromosomes and the 17 presumed ancestral bilaterian linkage groups at a level of conservation previously unseen, suggesting that the scallop may have a karyotype close to that of the bilaterian ancestor. Scallop Hox gene expression follows a new mode of subcluster temporal co-linearity that is possibly ancestral and may provide great potential in supporting diverse bilaterian body plans. Transcriptome analysis of scallop mantle eyes finds unexpected diversity in phototransduction cascades and a potentially ancient Pax2/5/8-dependent pathway for noncephalic eyes. The outstanding preservation of ancestral karyotype and developmental control makes the scallop genome a valuable resource for understanding early bilaterian evolution and biology.
Highlights
Reconstructing the genomes of bilaterian ancestors is central to our understanding of animal evolution, where knowledge from ancient and/or slow-evolving bilaterian lineages is critical
Ancient genomes may be reconstructed in both gene repertoire and genome organization through gene family studies and synteny analysis of high-order genome assemblies. In devoting such efforts to the scallop P. yessoensis, we find remarkable conservation of ancestral features in genome organization and gene repertoire that bring us closer to the bilaterian ancestral genome
These include the closest representation of the ancestral bilaterian karyotype to date, intact ParaHox and Hox gene clusters, diverse phototransduction cascades and an ancient regulatory pathway for eye development
Summary
Reconstructing the genomes of bilaterian ancestors is central to our understanding of animal evolution, where knowledge from ancient and/or slow-evolving bilaterian lineages is critical. Limited sequencing in the third group of protostome lophotrochozoans, a large superclade that includes molluscs, annelids and brachiopods, has revealed that their genomes are less derived from the ancestral bilaterian state than those of many ecdysozoans[5]. None of these lessderived lophotrochozoan genomes were assembled to a degree that permits chromosome-level genome comparison. Analysis of the scallop genome and extensive transcriptomes reveals outstanding preservation of ancestral bilaterian linkage groups, an intact Hox gene cluster under new expression control and diverse phototransduction cascades with a potentially ancient Pax2/5/8-dependent pathway for noncephalic eye formation, providing insights into the evolution of genome organization and developmental control during the emergence of bilaterians
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