Whole genome assembly and annotation of the King Angelfish (Holacanthus passer) gives insight into the evolution of marine fishes of the Tropical Eastern Pacific

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    Editors Assessment:

    The King Angelfish (Holacanthus passer) is a great example of a Holacanthus angelfish that are some of the most iconic marine fishes of the Tropical Eastern Pacific. However, very limited genomic resources currently exist for the genus and these authors have assembled and annotated the nuclear genome of the species, and used it examine the demographic history of the fish. Using nanopore long reads to assemble a compact 583 Mb reference with a contig N50 of 5.7 Mb, and 97.5% BUSCOs score. Scruitinising the data, the BUSCO score was high compared to the initial N50’s, providing some useful lessons learned on how to get the most out of ONT data. The analysis suggests that the demographic history in H. passer was likely shaped by historical events associated with the closure of the Isthmus of Panama, rather than by the more recent last glacial maximum. This data provides a genomic resource to improve our understanding of the evolution of Holacanthus angelfishes, and facilitating research into local adaptation, speciation, and introgression of marine fishes. In addition, this genome can help improve the understanding of the evolutionary history and population dynamics of marine species in the Tropical Eastern Pacific.

    This evaluation refers to version 1 of the preprint

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Abstract

Holacanthus angelfishes are some of the most iconic marine fishes of the Tropical Eastern Pacific (TEP). However, very limited genomic resources currently exist for the genus. In this study we: (i) assembled and annotated the nuclear genome of the King Angelfish (Holacanthus passer), and (ii) examined the demographic history of H. passer in the TEP. We generated 43.8 Gb of ONT and 97.3 Gb Illumina reads representing 75× and 167× coverage, respectively. The final genome assembly size was 583 Mb with a contig N50 of 5.7 Mb, which captured 97.5% of the complete Actinoterygii Benchmarking Universal Single-Copy Orthologs (BUSCOs). Repetitive elements accounted for 5.09% of the genome, and 33,889 protein-coding genes were predicted, of which 22,984 were functionally annotated. Our demographic analysis suggests that population expansions of H. passer occurred prior to the last glacial maximum (LGM) and were more likely shaped by events associated with the closure of the Isthmus of Panama. This result is surprising, given that most rapid population expansions in both freshwater and marine organisms have been reported to occur globally after the LGM. Overall, this annotated genome assembly provides a novel molecular resource to study the evolution of Holacanthus angelfishes, while facilitating research into local adaptation, speciation, and introgression in marine fishes.

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  1. Editors Assessment:

    The King Angelfish (Holacanthus passer) is a great example of a Holacanthus angelfish that are some of the most iconic marine fishes of the Tropical Eastern Pacific. However, very limited genomic resources currently exist for the genus and these authors have assembled and annotated the nuclear genome of the species, and used it examine the demographic history of the fish. Using nanopore long reads to assemble a compact 583 Mb reference with a contig N50 of 5.7 Mb, and 97.5% BUSCOs score. Scruitinising the data, the BUSCO score was high compared to the initial N50’s, providing some useful lessons learned on how to get the most out of ONT data. The analysis suggests that the demographic history in H. passer was likely shaped by historical events associated with the closure of the Isthmus of Panama, rather than by the more recent last glacial maximum. This data provides a genomic resource to improve our understanding of the evolution of Holacanthus angelfishes, and facilitating research into local adaptation, speciation, and introgression of marine fishes. In addition, this genome can help improve the understanding of the evolutionary history and population dynamics of marine species in the Tropical Eastern Pacific.

    This evaluation refers to version 1 of the preprint

  2. AbstractHolacanthus angelfishes are some of the most iconic marine fishes of the Tropical Eastern Pacific (TEP). However, very limited genomic resources currently exist for the genus. In this study we: i) assembled and annotated the nuclear genome of the King Angelfish (Holacanthus passer), and ii) examined the demographic history of H. passer in the TEP. We generated 43.8 Gb of ONT and 97.3 Gb Illumina reads representing 75X and 167X coverage, respectively. The final genome assembly size was 583 Mb with a contig N50 of 5.7 Mb, which captured 97.5% complete Actinoterygii Benchmarking Universal Single-Copy Orthologs (BUSCOs). Repetitive elements account for 5.09% of the genome, and 33,889 protein-coding genes were predicted, of which 22,984 have been functionally annotated. Our demographic model suggests that population expansions of H. passer occurred prior to the last glacial maximum (LGM) and were more likely shaped by events associated with the closure of the Isthmus of Panama. This result is surprising, given that most rapid population expansions in both freshwater and marine organisms have been reported to occur globally after the LGM. Overall, this annotated genome assembly will serve as a resource to improve our understanding of the evolution of Holacanthus angelfishes while facilitating novel research into local adaptation, speciation, and introgression in marine fishes.

    This work has been published in GigaByte Journal under a CC-BY 4.0 license (https://doi.org/10.46471/gigabyte.115), and has published the reviews under the same license. These are as follows.

    Reviewer 1. Iria Fernandez Silva

    Is the language of sufficient quality? Yes. But, A "the" is missing before "clingfish" in line 171

    Additional Comments:

    The genome assembly presented is of high quality, with values of accuracy and completeness in pair with chromosome level assemblies. The study is very well presented in terms on quality of the results and clarity in the presentation of methods and results. An added value is that it allows understanding how different type of data and assemblers interact in improvng the assembly quality. I also found interesting to see how contiguity and completeness are not always correlated, as this assembly has a great completeness BUSCO score in spite of not having the greatest N50 (compared with the most modern assemblies). This is possibly inherent to the type of data (ONT reads) and this information may guide researchers in making decission over future assembly projects. The demographic analysis is a nice addition to the study, the results are coherent and add information interesting to study the evolution of reef fishes and the biogeography of the TEP. I would appeciate more detail in the captions of figure 4, particularly those of the figure 4D.

    Reviewer 2. Yue Song

    The sequencing and annotation of King Angelfish genomes is impressive and represents a significant addition to the genomic resources for marine fishes. By hybrid assembly, a high-quality genome was provided, and the relationship between historical dynamics of its population and geological events was further discussed. However, in the section on inferring the demographic history, there is no mention of how the author inferred the mutation rate of this species. In addition, the author obtained 486 contigs throughout the assembly using ONT data combined with short reads. Is it possible to further assemble these contigs into chromosomal level? Of course, this does not indicate that it must be achieved within this manuscript, but rather suggests the inclusion of additional discussion on methods to further enhance the referential value of this genome. Additional specific comments: (1) Line 86, I guess the author probably meant to say there were 486 contigs, right? (2) Line 294, "gene models", not "gen models" (3) Line 110-111, it is puzzled my about the numbers in parentheses. I don't quite understand what these numbers mean. I haven't seen any explanation in this MS. Did I miss something? (4) If possible, it is recommended to show the phylogenetic relationships between these species in Figure 3.