Still waters run deep: Large scale genome rearrangements in the evolution of morphologically conservative Polyplacophora

Abstract

Abstract The phylum Mollusca is bifurcated into the hyperdiverse Conchifera (Gastropoda, Bivalvia, Cephalopoda, et al.) and the spiny Aculifera (Polyplacophora and Aplacophora). High quality genomic data for the deeply divergent, morphologically constrained chitons, would be expected to offer an opportunity to explore ancient genetic traits and evolutionary mechanisms preserved across the long span of animal evolution. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades: Lepidopleurida ( Deshayesiella sirenkoi ), Callochitonida ( Callochiton septemvalvis ) and Chitonida ( Acanthochitona discrepans and A. rubrolineata ), and an updated phylogeny for the phylum. Comparison with conchiferan genomes recovers 20 ancient molluscan linkage groups (MLGs) that are relatively conserved in bivalve karyotypes, but subject to re-ordering, rearrangement, fusion, and early occurring duplication (or fission) in chitons and conchiferan genomes. Two congeners each have 8 haploid chromosomes, results of two independent fusion events from the karyotype of their most recent common ancestor. The largest number of novel fusions is in the supposedly most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the known occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals and is not explained by accumulated change since the deep divergence time of this clade. The apparently conservative phenome of chitons is not reflected in a conservative genome.