The “fossil” genome of scallop Patinopecten yessoensis

Identifying and charactering the bilaterian ancestors is central to our understanding of early animal evolution but hindered by the incompleteness of fossil records. In the absence of definitive fossil records, genomic reconstruction becomes essential to our understanding of early bilaterian ancestors and their subsequent evolution, where knowledge from ancient and/or slow-evolving bilaterian lineages is critical. We finished a high-quality, chromosome-anchored reference genome for scallop Patinopecten yessoensis. 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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Apr 04, 2017
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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. Our current understanding of bilaterian genome evolution largely depends on genome sampling from two major bilaterian groups (Deuterostomia and Ecdysozoa), whereas the third group Lophotrochozoa including molluscs, annelids and brachiopods remains genomically poorly explored. Recent studies reveal that lophotrochozoan genomes are less derived from the ancestral bilaterian state than those of many ecdysozoans [1]. Deep sampling of genomes of lophotrochozoan lineages close to the root of bilaterians may enhance our understanding of early bilaterian ancestors and their subsequent evolution.

In 2012, we started the scallop genome sequencing project, and our initial goals were to investigate its molecular adaptations to semi-sessile lifestyle. But when we obtained and first looked at the genome of scallop Patinopecten yessoensis (a species of the bivalve lineage with earliest fossil records dating back to early Cambrian), we were shocked by its astonishing preservation of the bilaterian ancestral genes and ancestral linkage groups. The scallop genome retains more ancestral gene families than any other bilaterian genomes sequenced so far. A near-perfect correspondence is found between the 19 scallop chromosomes and the 17 presumed ancestral bilaterian linkage groups [1], suggesting that scallop may have a karyotype close to that of the bilaterian ancestor. The conservative feature of scallop karyotype is also supported by the finding of remarkable conservation of the linkage of representative gene families (e.g. Hox cluster, ParaHox cluster and NK cluster) in the scallop genome. We feel that we have discovered a “fossil” genome that may closely resembles that of the bilaterian ancestor in both gene content and karyotype.

Further investigation of the scallop genome also provides novel insights in the evolution of body plan and the eye, Darwin’s “organ of extreme perfection”. We find that the Hox gene cluster in the scallop follows a novel subcluster temporal co-linearity (STC) that may be ancestral to whole cluster co-linearity as observed in vertebrates. Owing to its increased flexibility in developmental patterning, STC may be central to the bilaterian body plan evolution and may provide the bilaterian ancestor with great potential in generating diverse body plans found in molluscs and other bilaterian lineages. Our view is in fact supported by a recent interesting study showing that differential activation of trunk-patterning Hox genes can result in different larval body plans of direct and indirect developing hemichordates [2]. Analysis of scallop mantle eyes reveals unexpected diversity in phototransduction cascades (mediated by r-opsins, Go-opsins and c-opsins), and Pax2/5/8 but not Pax6 as the key regulator in the eye gene network, supporting different evolutionary origins of cephalic and noncephalic eyes [3] and arguing against Pax6 as the universal master control gene for all bilaterian eyes [4].

Our analyses of the “fossil” genome of scallop along with the finding of the earliest fossil bilaterian Kimberella as mollusc-like [5], suggest that bivalve molluscs are excellent evolutionary models for study, and further investigation of this and other ancient molluscan lineages may greatly improve our understanding of early bilaterian evolution.

The paper is available here: http://go.nature.com/2nSpEIs

References

  1. Simakov, O. et al. Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526-531 (2013).
  2. Gonzalez, P., Uhlinger K. R. & Lowe, C. J. The adult body plan of indirect developing hemichordates develops by adding a Hox-patterned trunk to an anterior larval territory. Curr. Biol. 27, 1-9 (2017).
  3. Backfisch, B. et al. Stable transgenesis in the marine annelid Platynereis dumerilii sheds new light on photoreceptor evolution. Proc. Natl. Acad. Sci. USA 110, 193-198 (2013).
  4. Gehring, W. J. & Ikeo, K. Pax6: mastering eye morphogenesis and eye evolution. Trends Genet. 15, 371-377 (1999).
  5. Fedonkin, M. A. & Waggoner, B. M. The Late Precambrian fossil Kimberella is a mollusc-like bilaterian organism. Nature 388, 868–871 (1997).

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Shi Wang

Professor, Ocean University of China

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