Many molluscan genomes have been published to date, however only three are from representatives of the subphylum Aculifera (Polyplacophora, Caudofoveata, and Solenogastres), the sister taxon to all other molluscs. Currently, genomic resources are completely lacking for Solenogastres. This gap in knowledge hinders comparative and evolutionary studies. Here, we sequenced the genomes of the solenogaster aplacophoransEpimenia babai Salvini-Plawen, 1997 andNeomenia megatrapezata Salvini-Plawen & Paar-Gausch, 2004 using a hybrid approach combining Oxford Nanopore and Illumina reads. ForE. babai , we produced a 628 Mbp haploid assembly (N50 = 413 Kbp, L50 = 370) that is rather complete with a BUSCO completeness score of 90.1% (82.0% single, 8.1% duplicated, 6.0% fragmented, and 3.9% missing). ForN. megatrapezata , we produced a 412 Mbp haploid assembly (N50 = 132 Kbp, L50 = 881) that is also rather complete with a BUSCO completeness score of 85.1% (81.7% single, 3.4% duplicated, 8.1% fragmented, and 6.8% missing). Our annotation pipeline predicted 25,393 gene models forE. babai with a BUSCO score of 92.4% (80.5% single, 11.9% duplicated, 4.9% fragmented, and 2.7% missing) and 22,463 gene models forN. megatrapezata with a BUSCO score of 90.2% (81.0% single, 9.2% duplicated, 4.7% fragmented, and 5.1% missing). Phylogenomic analysis recovered Solenogastres as the sister taxon to Polyplacophora and Aculifera as the sister taxon to all other sampled molluscs with maximal support. These represent the first whole-genome resources for Solenogastres and will be valuable for future studies investigating this understudied group and molluscan evolution as a whole.
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Genome of the lepidopleurid chiton Hanleya hanleyi (Mollusca, Polyplacophora)
Mollusca is the second most species-rich phylum and includes animals as disparate as octopuses, clams, and chitons. Dozens of molluscan genomes are available, but only one representative of the subphylum Aculifera, the sister taxon to all other molluscs, has been sequenced to date, hindering comparative and evolutionary studies. To facilitate evolutionary studies across Mollusca, we sequenced the genome of a second aculiferan mollusc, the lepidopleurid chiton Hanleya hanleyi (Bean 1844), using a hybrid approach combining Oxford Nanopore and Illumina reads. After purging redundant haplotigs and removing contamination from this 1.3% heterozygous genome, we produced a 2.5 Gbp haploid assembly (>4X the size of the other chiton genome sequenced to date) with an N50 of 65.0 Kbp. Despite a fragmented assembly, the genome is rather complete (92.0% of BUSCOs detected; 79.4% complete plus 12.6% fragmented). Remarkably, the genome has the highest repeat content of any molluscan genome reported to date (>66%). Our gene annotation pipeline predicted 69,284 gene models (92.9% of BUSCOs detected; 81.8% complete plus 11.1% fragmented) of which 35,362 were supported by transcriptome and/or protein evidence. Phylogenomic analysis recovered Polyplacophora sister to all other sampled molluscs with maximal support. The Hanleya genome will be a valuable resource for studies of molluscan biology with diverse potential applications ranging from evolutionary and comparative genomics to molecular ecology.
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- Award ID(s):
- 1846174
- PAR ID:
- 10424517
- Date Published:
- Journal Name:
- F1000Research
- Volume:
- 11
- ISSN:
- 2046-1402
- Page Range / eLocation ID:
- 555
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)Choosing the optimum assembly approach is essential to achieving a high-quality genome assembly suitable for comparative and evolutionary genomic investigations. Significant recent progress in long-read sequencing technologies such as PacBio and Oxford Nanopore Technologies (ONT) has also brought about a large variety of assemblers. Although these have been extensively tested on model species such as Homo sapiens and Drosophila melanogaster , such benchmarking has not been done in Mollusca, which lacks widely adopted model species. Molluscan genomes are notoriously rich in repeats and are often highly heterozygous, making their assembly challenging. Here, we benchmarked 10 assemblers based on ONT raw reads from two published molluscan genomes of differing properties, the gastropod Chrysomallon squamiferum (356.6 Mb, 1.59% heterozygosity) and the bivalve Mytilus coruscus (1593 Mb, 1.94% heterozygosity). By optimizing the assembly pipeline, we greatly improved both genomes from previously published versions. Our results suggested that 40–50X of ONT reads are sufficient for high-quality genomes, with Flye being the recommended assembler for compact and less heterozygous genomes exemplified by C. squamiferum , while NextDenovo excelled for more repetitive and heterozygous molluscan genomes exemplified by M. coruscus . A phylogenomic analysis using the two updated genomes with 32 other published high-quality lophotrochozoan genomes resulted in maximum support across all nodes, and we show that improved genome quality also leads to more complete matrices for phylogenomic inferences. Our benchmarking will ensure efficiency in future assemblies for molluscs and perhaps also for other marine phyla with few genomes available. This article is part of the Theo Murphy meeting issue ‘Molluscan genomics: broad insights and future directions for a neglected phylum’.more » « less
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Body size is a fundamental characteristic of animals that impacts every aspect of their biology from anatomical complexity to ecology. In Mollusca, Solenogastres has been considered important to understanding the group’s early evolution as most morphology-based phylogenetic reconstructions placed it as an early branching molluscan lineage. Under this scenario, molluscs were thought to have evolved from a small, turbellarian-like ancestor and small (i.e., macrofaunal) body size was inferred to be plesiomorphic for Solenogastres. More recently, phylogenomic studies have shown that aplacophorans (Solenogastres + Caudofoveata) form a clade with chitons (Polyplacophora), which is sister to all other molluscs, suggesting a relatively large-bodied (i.e., megafaunal) ancestor for Mollusca. Meanwhile, recent investigations into aplacophoran phylogeny have called the assumption that the last common ancestor of Solenogastres was small-bodied into question, but sampling of meiofaunal species was limited, biasing these studies towards large-bodied taxa and leaving fundamental questions about solenogaster body size evolution unanswered. Here, we supplemented available data with transcriptomes from eight diverse meiofaunal species of Solenogastres and conducted phylogenomic analyses on datasets of up to 949 genes. Maximum likelihood analyses support the meiofaunal family Meiomeniidae as the sister group to all other solenogasters, congruent with earlier ideas of a small-bodied ancestor of Solenogastres. In contrast, Bayesian Inference analyses support the large-bodied family Amphimeniidae as the sister group to all other solenogasters. Investigation of phylogenetic signal by comparing site-wise likelihood scores for the two competing hypotheses support the Meiomeniidae-first topology. In light of these results, we performed ancestral character state reconstruction to explore the implications of both hypotheses on understanding of Solenogaster evolution and review previous hypotheses about body size evolution and its potential consequences for solenogaster biology. Both hypotheses imply that body size evolution has been highly dynamic over the course of solenogaster evolution and that their relatively static body plan has successfully allowed for evolutionary transitions between meio-, macro- and megafaunal size ranges.more » « less
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Abstract Relationships among the major lineages of Mollusca have long been debated. Morphological studies have considered the rarely collected Monoplacophora (Tryblidia) to have several plesiomorphic molluscan traits. The phylogenetic position of this group is contentious as morphologists have generally placed this clade as the sister taxon of the rest of Conchifera whereas earlier molecular studies supported a clade of Monoplacophora + Polyplacophora (Serialia) and phylogenomic studies have generally recovered a clade of Monoplacophora + Cephalopoda. Phylogenomic studies have also strongly supported a clade including Gastropoda, Bivalvia, and Scaphopoda, but relationships among these taxa have been inconsistent. In order to resolve conchiferan relationships and improve understanding of early molluscan evolution, we carefully curated a high-quality data matrix and conducted phylogenomic analyses with broad taxon sampling including newly sequenced genomic data from the monoplacophoran
Laevipilina antarctica . Whereas a partitioned maximum likelihood (ML) analysis using site-homogeneous models recovered Monoplacophora sister to Cephalopoda with moderate support, both ML and Bayesian inference (BI) analyses using mixture models recovered Monoplacophora sister to all other conchiferans with strong support. A supertree approach also recovered Monoplacophora as the sister taxon of a clade composed of the rest of Conchifera. Gastropoda was recovered as the sister taxon of Scaphopoda in most analyses, which was strongly supported when mixture models were used. A molecular clock based on our BI topology dates diversification of Mollusca to ~546 MYA (+/− 6 MYA) and Conchifera to ~540 MYA (+/− 9 MYA), generally consistent with previous work employing nuclear housekeeping genes. These results provide important resolution of conchiferan mollusc phylogeny and offer new insights into ancestral character states of major mollusc clades. -
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.12688/f1000research.121706.1
