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The queen conch mitogenome: intra- and interspecific mitogenomic variability in Strombidae and phylogenetic considerations within the Hypsogastropoda.

ABSTRACT: Aliger gigas is an economically important and vulnerable marine species. We present a new mitogenome of A. gigas from the Mexican Caribbean and use the eight publicly available Strombidae mitogenomes to analyze intra- and interspecific variation. We present the most complete phylogenomic understanding of Hypsogastropoda to date (17 superfamilies, 39 families, 85 genera, 109 species) to revisit the phylogenetic position of the Stromboidea and evaluate divergence times throughout the phylogeny. The A. gigas mitogenome comprises 15,460 bp including 13 PCGs, 22 tRNAs, and two rRNAs. Nucleotide diversity suggested divergence between the Mexican and Colombian lineages of A. gigas. Interspecific divergence showed high differentiation among Strombidae species and demonstrated a close relationship between A. gigas and Strombus pugilis, between Lambis lambis and Harpago chiragra, and among Tridentarius dentatus/Laevistrombus canarium/Ministrombus variabilis. At the intraspecific level, the gene showing the highest differentiation is ATP8 and the lowest is NAD4L, whereas at the interspecific level the NAD genes show the highest variation and the COX genes the lowest. Phylogenomic analyses confirm that Stromboidea belongs in the non-Latrogastropoda clade and includes Xenophoridea. The phylogenomic position of other superfamilies, including those of previously uncertain affiliation, is also discussed. Finally, our data indicated that Stromboidea diverged into two principal clades in the early Cretaceous while Strombidae diversified in the Paleocene, and lineage diversification within A. gigas took place in the Pleistocene.

SUBMITTER: Machkour-M'Rabet S

PROVIDER: S-EPMC8184947 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Stylommatophora is one of the most speciose orders of Gastropoda, including terrestrial snails and slugs, some of which are economically important as human food, agricultural pests, vectors of parasites or due to invasiveness. Despite their great diversity and relevance, the internal phylogeny of Stylommatophora has been debated. To date, only 34 stylommatophoran mitogenomes were sequenced. Here, the complete mitogenome of an invasive pest slug, Arion vulgaris Moquin-Tandon, 1855 (Stylommatophora: Arionidae), was sequenced using next generation sequencing, analysed and compared with other stylommatophorans. The mitogenome of A. vulgaris measures 14,547 bp and contains 13 protein-coding, two rRNA, 22 tRNA genes, and one control region, with an A + T content of 70.20%. All protein coding genes (PCGs) are initiated with ATN codons except for COX1, ND5 and ATP8 and all are ended with TAR or T-stop codons. All tRNAs were folded into a clover-leaf secondary structure except for trnC and trnS1 (AGN). Phylogenetic analyses confirmed the position of A. vulgaris within the superfamily Arionoidea, recovered a sister group relationship between Arionoidea and Orthalicoidea, and supported monophyly of all currently recognized superfamilies within Stylommatophora except for the superfamily Helicoidea. Initial diversification time of the Stylommatophora was estimated as 138.55 million years ago corresponding to Early Cretaceous. The divergence time of A. vulgaris and Arion rufus (Linnaeus, 1758) was estimated as 15.24 million years ago corresponding to one of Earth's most recent, global warming events, the Mid-Miocene Climatic Optimum. Furthermore, selection analyses were performed to investigate the role of different selective forces shaping stylommatophoran mitogenomes. Although purifying selection is the predominant selective force shaping stylommatophoran mitogenomes, six genes (ATP8, COX1, COX3, ND3, ND4 and ND6) detected by the branch-specific aBSREL approach and three genes (ATP8, CYTB and ND4L) detected by codon-based BEB, FUBAR and MEME approaches were exposed to diversifying selection. The positively selected substitutions at the mitochondrial PCGs of stylommatophoran species seems to be adaptive to environmental conditions and affecting mitochondrial ATP production or protection from reactive oxygen species effects. Comparative analysis of stylommatophoran mitogenome rearrangements using MLGO revealed conservatism in Stylommatophora; exceptions refer to potential apomorphies for several clades including rearranged orders of trnW-trnY and of trnE-trnQ-rrnS-trnM-trnL2-ATP8-trnN-ATP6-trnR clusters for the genus Arion. Generally, tRNA genes tend to be rearranged and tandem duplication random loss, transitions and inversions are the most basic mechanisms shaping stylommatophoran mitogenomes.

Project description:BackgroundQueen conch (Strombus gigas) reproduction is inhibited in nearshore areas of the Florida Keys, relative to the offshore environment where conchs reproduce successfully. Nearshore reproductive failure is possibly a result of exposure to environmental factors, including heavy metals, which are likely to accumulate close to shore. Metals such as Cu and Zn are detrimental to reproduction in many mollusks.Methodology/principal findingsHistology shows gonadal atrophy in nearshore conchs as compared to reproductively healthy offshore conchs. In order to determine molecular mechanisms leading to tissue changes and reproductive failure, a microarray was developed. A normalized cDNA library for queen conch was constructed and sequenced using the 454 Life Sciences GS-FLX pyrosequencer, producing 27,723 assembled contigs and 7,740 annotated transcript sequences. The resulting sequences were used to design the microarray. Microarray analysis of conch testis indicated differential regulation of 255 genes (p<0.01) in nearshore conch, relative to offshore. Changes in expression for three of four transcripts of interest were confirmed using real-time reverse transcription polymerase chain reaction. Gene Ontology enrichment analysis indicated changes in biological processes: respiratory chain (GO:0015992), spermatogenesis (GO:0007283), small GTPase-mediated signal transduction (GO:0007264), and others. Inductively coupled plasma-mass spectrometry analysis indicated that Zn and possibly Cu were elevated in some nearshore conch tissues.Conclusions/significanceCongruence between testis histology and microarray data suggests that nearshore conch testes regress during the reproductive season, while offshore conch testes develop normally. Possible mechanisms underlying the testis regression observed in queen conch in the nearshore Florida Keys include a disruption of small GTPase (Ras)-mediated signaling in testis development. Additionally, elevated tissue levels of Cu (34.77 ng/mg in testis) and Zn (831.85 ng/mg in digestive gland, 83.96 ng/mg in testis) nearshore are similar to reported levels resulting in reproductive inhibition in other gastropods, indicating that these metals possibly contribute to NS conch reproductive failure.

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The queen conch mitogenome: intra- and interspecific mitogenomic variability in Strombidae and phylogenetic considerations within the Hypsogastropoda.

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