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Generation of Large Mitochondrial and Nuclear Nucleotide Sequences And MOLLUSCAN RESEARCH https://doi.org/10.1080/13235818.2021.1957552 Generation of large mitochondrial and nuclear nucleotide sequences and phylogenetic analyses using high-throughput short-read datasets for endangered Placostylinae snails of the southwest Pacific Mathieu Quenu , Steven A. Trewick, Elizabeth E. Daly and Mary Morgan-Richards Wildlife & Ecology, School of Agriculture & Environment, College of Sciences, Massey University, Palmerston North, New Zealand ABSTRACT KEYWORDS Placostylinae are a sub-family of terrestrial land snails endemic to the southwest Pacific. Some Histone genes; genetic species are harvested for food, and others are critically endangered. Here we assemble and resources; mitochondrial characterise complete mitochondrial genomes, as well as three nuclear markers (partial 45S genome; phylogenetics; ribosomal cassettes and the histone genes H3 and H4) of five snail species from three Placostylus; ribosomal cassette geographical regions (New Zealand, New Caledonia and the Solomon Islands). Mitogenomes of Placostylinae snails ranged between 14,544 bp and 14,711 bp, with minor variation in the position of tRNA tyrosine (Y) and tRNA tryptophane (W). The 45S ribosomal cassette contained intra-genomic nucleotide variation in ITS2. Cassettes containing histone genes H3 and H4 and their non-transcribed spacer region were assembled for three species, with the two genes coded in the same direction. Phylogenetic analysis on this large dataset (mitochondrial genome + nuclear markers) supported geographical clustering of species but could not confidently infer monophyly of the four Placostylus species with respect to Eumecostylus cleryi. Analysis based on shorter cytochrome c oxidase sequences with a wider taxon sampling found species representing the genera Eumecostylus and Placocharis were nested within the phylogenetic diversity of Placostylus. Multi-locus phylogenetic analysis containing mitochondrial and nuclear sequences did not support monophyly of Placostylinae. Introduction phylogenetic signal. They are, however, associated With approximately 85,000 recognised extant species, with a high methodological cost and require either Mollusca is the second most diverse animal phylum the generation of transcriptomic data in parallel to on earth (MolluscaBase eds. 2021). Systematics within generation of genomic libraries (exon-based recap- this phylum still need improvement, and many ture) or the use of probes to enrich genomic datasets species complexes are yet to be fully described or in regions of interest (anchored phylogenomics). One understood (Lydeard et al. 2004). Molecular tools can simpler phylogenomic approach is to use mitochon- be used to identify management units and comp- drial and multi-copy nuclear gene data reconstructed lement morphological data (Moritz 1994). Short DNA from genomic libraries as input for phylogenetic analy- sequences have been widely used for inferring phylo- sis. Both types of markers are overrepresented in genetic relationships among molluscs in the last few shotgun sequencing genomic libraries and therefore decades (e.g., Wade et al. 2006; Herbert and Mitchell the methodological and economical cost associated 2009; Ramirez et al. 2009), but the emergence of with their generation is minimal. In addition, because high-throughput Next Generation Sequencing (NGS) they are present in high numbers they will usually be technology has made it possible to analyse signifi- a good target in analysis of fossil shells, which are cantly larger genetic data sets (Hunter et al. 2016). now providing opportunities to incorporate ancient For phylogenetic inferences to be reliable, genomic DNA into tests of evolutionary change through phylo- regions targeted by NGS technologies must be both genetic analysis (Daly et al. 2020; Der Sarkissian et al. conserved enough to allow sequence alignment and 2020; Ferreira et al. 2020). Here we use high-through- at the same time display enough nucleotide variation put short-read sequencing to assemble whole mito- to permit inference of statistically robust phylogenetic chondrial genomes, 45S nuclear ribosomal DNA relationships. Technologies such as exon-based recap- cassettes and the histone genes H3 and H4 of five ture (Teasdale et al. 2016) or anchored phylogenomics species of Placostylinae Pilsbry, 1946, a sub-family of (Lemmon and Lemmon 2012) can now be used to giant terrestrial land snails endemic to the southwest sample up to hundreds of genomic regions with Pacific region. We use these data to infer phylogenetic CONTACT Mathieu Quenu [email protected] Wildlife & Ecology, School of Agriculture & Environment, College of Sciences, Massey University, Private Bag 11-222, Palmerston North 4442, New Zealand Supplemental data for this article can be accessed at https://doi.org/10.1080/13235818.2021.1957552. © 2021 The Malacological Society of Australasia and the Society for the Study of Molluscan Diversity Published online 01 Aug 2021 2 M. QUENU ET AL. relationships among Placostylinae species living on the faster evolving mtDNA NADH dehydrogenase 2 separate islands, and among other related species. (ND2) gene in combination with shell shape analysis The Placostylinae belong to the superfamily Ortha- and nuclear SNP markers to explore population level licoidea (Breure et al. 2010; Breure and Romero 2012) diversity (Dowle et al. 2015). Deeper phylogenetic and contain among others the three genera Placostylus relationships have also been investigated within the (H. Beck, 1837), Eumecostylus (Martens in Albers, 1860) superfamily Orthalicoidea using concatenated short and Placocharis (Pilsbry, 1900) that are endemic to DNA sequences (Breure and Romero 2012), including islands in the southwest Pacific. Most of the recognised data from P. ambagiosus from New Zealand, Placostylus species in these genera live on Melanesian islands from eddystonensis (Pfeiffer, 1855) from New Caledonia, and the Bismarck and Solomon archipelagos to Vanuatu, Eumecostylus uligunosus (Kobelt, 1891) and Placocharis New Caledonia and Fiji but also on islands further strangei (Pfeiffer, 1855) from the Solomon Islands. The south (Lord Howe, Three Kings, and the Far North of 2079 bp alignment of concatenated sequence (COXI, New Zealand). Many of these snail taxa are under ITS2/28S, Histone H3) supported the Placostylinae as threat of extinction from anthropogenic habitat a clade within the Bothriembryontidae. change and predator introduction, and some are Until now, no full mitochondrial genome or 45S already considered extinct (Brescia et al. 2008; Stringer ribosomal RNA cassette has been assembled for any et al. 2014). In many places extensive fossil deposits of Placostylinae species, and the gene arrangement of Placostylus provide a potential resource for studies of histone H3 and H4 genes is not known. Mitochondrial changing environmental conditions (Brook 1999). In DNA occurs in high copy numbers and therefore is New Caledonia at least six species are recognised likely to be most appropriate for ancient DNA studies (Dowle et al. 2015) and they are culturally and econ- from fossil shells (Shtolz and Mishmar 2019). Nuclear omically important as food (Quenu et al. 2020). On 45S ribosomal cassettes, which include the conserved Grande Terre itself, the main island of New Caledonia, regions 18S, 5.8S, 28S and the unconstrained Internal Placostylus populations have declined and some Transcribed Spacers 1 and 2 (ITS1 and ITS2), are species are at risk (Brescia et al. 2008), but on Île Des multi-copy. The ribosomal subunits 18S, 5.8S and 28S Pins (Isle of Pines) just south of Grande Terre, Placosty- are conserved by their function in the translation of lus snails are still harvested for food by indigenous cytoplasmic mRNA of eukaryotic cells (Kressler et al. Kanak people. New Zealand Placostylus species are 2010). ITS1 and ITS2 separate the different subunits considered vulnerable and today survive only in within the 45S cassette and their nucleotide sequences highly fragmented remnant colonies (Parrish et al. are highly variable. The 45S ribosomal cassettes are 1995; Daly et al. 2020). On Lord Howe Island, Placosty- present in numerous tandem copies, usually on lus bivaricosus (Gaskoin, 1855) is critically endangered several chromosomes in the nuclear genome (Dalet (Ponder et al. 2003). On other island systems such as et al. 2014), and are thought to evolve via concerted Fiji and the Solomon Islands Placostylinae are subject evolution (Nei and Rooney 2005). Intra-individual vari- to similar threats, although information on these popu- ation of nucleotide sequences is common in ITS, and lations is limited (Brodie 2012). can produce statistical noise when ITS sequences are Previous molecular work on Placostylinae has relied used in phylogenetic or population genetic analysis on application of universal PCR primers to target short (Hillis and Dixon 1991; Nei and Rooney 2005; Sochor- fragments (<850 bp) of mitochondrial genes. Using ová et al. 2018). The two histone genes H3 and H4 partial mtDNA cytochrome c oxidase subunit 1 (COXI) code for protein subunits of the nucleosome sequences, the Lord Howe species, P. bivaricosus complex. They are usually linked by a noncoding (Gaskoin, 1855), was identified as sister to the two spacer region, and in molluscs they have been New Zealand mainland species, Placostylus ambagiosus reported to be coded on opposing strands in some (Suter, 1906) and Placostylus hongii (Lesson, 1830), species (Armbruster et al. 2005; Harl et al. 2014), but while the third New Zealand
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