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

Reviewer #1 (Public review):

Summary of Key Findings:

The authors identified 20 ancient molluscan linkage groups (MLGs) that are largely conserved in other molluscan groups but highly dynamic and rearranged in chitons. This contrasts with the stability seen in other animal groups.

Significant chromosome rearrangements, fusions, and duplications were observed in chitons, particularly in the most basal clades like Lepidopleurida, indicating that chitons undergo more extensive genomic changes than expected.

Chitons exhibit extremely high levels of genomic heterozygosity, exceeding that of other molluscan species and even Lepidoptera. This presents challenges for assembling high-quality genomes but also points to genetic diversity as a driver of evolutionary processes.

Partial genome duplications, particularly in Liolophura japonica, extend the knowledge of gene duplication events within the broader Mollusca clade.

The paper speculates that these genomic rearrangements may contribute to maintaining species boundaries in sympatric and parapatric radiations, as observed in certain Acanthochitona species.

Strengths:

The use of high-quality genomic data, including four de novo genome assemblies, provides robust evidence for the conclusions.

The research challenges the common assumption that chitons are evolutionarily conservative, showing that their genomes are highly dynamic despite their morphological stasis.

The study adds to the understanding of how chromosomal rearrangements might contribute to speciation, a concept that can be applied to other taxa.

Limitations:

The paper acknowledges that the limited availability of high-quality genomes across molluscs may restrict the scope of comparative analyses. More genomic data from other molluscan groups could strengthen the conclusions.

The role of high heterozygosity in chitons is highlighted, but more information is needed to clarify how this affects genome assembly and evolutionary outcomes.

Implications for Future Research:

The research raises important questions about the relationship between genomic instability and phenotypic stasis, which can inform studies in other animal groups.

The findings call for a re-evaluation of how we define and measure biodiversity, particularly in "neglected" clades like chitons. Further studies could focus on linking the observed genomic changes to specific adaptive traits or ecological niches.

Reviewer #2 (Public review):

Summary:

The authors provide four new annotated genomes for an important taxon within Mollusca known as Polyplacophora (chitons). They provide an impressive analysis showing syntenic relationships between the chromosomes of these four genomes but also other available chiton genome sequences and analysis of 20 molluscan linkage groups to expand this analysis across Mollusca.

Strengths:

The authors have selected particular chiton species for genome sequencing and annotation that expand what is known about genomes across portions of chiton phylogenetic diversity lacking genome sequences. The manuscript is well-written and illustrated in a concise manner. The figures are mostly clear, allowing a reader to visually compare the syntenic relationships of chromosomes, especially within chitons. Their phylogenetic analysis provides a simple manner to map important events in molluscan genome evolution. This study greatly expands what is known about molluscan and chiton comparative genomics.

Weaknesses:

I am not especially convinced that chitons have experienced more substantial genomic rearrangements or other genomic events than other molluscan classes, and for this reason, I did not personally find the title compelling: "Still waters run deep: Large scale genome rearrangements in the evolution of morphologically conservative Polyplacophora." Are the documented events "large scale genomic rearrangements"? It seems that mostly they found two cases of chromosome fusion, plus one apparent case of whole genome duplication. What do they mean by "Still waters run deep"? I have no idea. I guess they consider chitons to be morphologically conservative in their appearance and lifestyle so they are calling attention to this apparent paradox. However, most chiton genomes seem to be relatively conserved, but there are unexpected chromosome fusion events within a particular genus, Acanthochitona. Likewise, they found a large-scale gene duplication event in Acanthopleurinae, a different subfamily of chitons, which is quite interesting but these seem to be geologically recent events that do not especially represent the general pattern of genome evolution across this ancient molluscan taxon.