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Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents.

ABSTRACT: Aim:Identification of the processes that generate and maintain species diversity within the same region can provide insight into biogeographic patterns at broader spatiotemporal scales. Hawkfishes in the genus Paracirrhites are a unique taxon to explore with respect to niche differentiation, exhibiting diagnostic differences in coloration, and an apparent center of distribution outside of the Indo-Malay-Philippine (IMP) biodiversity hotspot for coral reef fishes. Our aim is to use next-generation sequencing methods to leverage samples of a taxon at their center of maximum diversity to explore phylogenetic relationships and a possible mechanism of coexistence. Location:Flint Island, Southern Line Islands, Republic of Kiribati. Methods:A comprehensive review of museum records, the primary literature, and unpublished field survey records was undertaken to determine ranges for four "arc-eye" hawkfish species in the Paracirrhites species complex and a potential hybrid. Fish from four Paracirrhites species were collected from Flint Island in the Southern Line Islands, Republic of Kiribati. Hindgut contents were sequenced, and subsequent metagenomic analyses were used to assess the phylogenetic relatedness of the host fish, the microbiome community structure, and prey remains for each species. Results:Phylogenetic analyses conducted with recovered mitochondrial genomes revealed clustering of P. bicolor with P. arcatus and P. xanthus with P. nisus, which were unexpected on the basis of previous morphological work in this species complex. Differences in taxonomic composition of gut microbial communities and presumed prey remains indicate likely separation of foraging niches. Main Conclusions:Our findings point toward previously unidentified relationships in this cryptic species complex at its proposed center of distribution. The three species endemic to the Polynesian province (P. nisus, P. xanthus, and P. bicolor) cluster separately from the more broadly distributed P. arcatus on the basis of relative abundance of metazoan sequences in the gut (presumed prey remains). Discordance between gut microbial communities and phylogeny of the host fish further reinforce the hypothesis of niche separation.

SUBMITTER: French BJ

PROVIDER: S-EPMC7141070 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents.

French Beverly J BJ Lim Yan Wei YW Zgliczynski Brian J BJ Edwards Robert A RA Rohwer Forest F Sandin Stuart A SA

Ecology and evolution 20200310 7

<h4>Aim</h4>Identification of the processes that generate and maintain species diversity within the same region can provide insight into biogeographic patterns at broader spatiotemporal scales. Hawkfishes in the genus <i>Paracirrhites</i> are a unique taxon to explore with respect to niche differentiation, exhibiting diagnostic differences in coloration, and an apparent center of distribution outside of the Indo-Malay-Philippine (IMP) biodiversity hotspot for coral reef fishes. Our aim is to use ...[more]

PMID: 32273998

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Project description:IntroductionThe PCR-based analysis of homologous genes has become one of the most powerful approaches for species detection and identification, particularly with the recent availability of Next Generation Sequencing platforms (NGS) making it possible to identify species composition from a broad range of environmental samples. Identifying species from these samples relies on the ability to match sequences with reference barcodes for taxonomic identification. Unfortunately, most studies of environmental samples have targeted ribosomal markers, despite the fact that the mitochondrial Cytochrome c Oxidase subunit I gene (COI) is by far the most widely available sequence region in public reference libraries. This is largely because the available versatile ("universal") COI primers target the 658 barcoding region, whose size is considered too large for many NGS applications. Moreover, traditional barcoding primers are known to be poorly conserved across some taxonomic groups.ResultsWe first design a new PCR primer within the highly variable mitochondrial COI region, the "mlCOIintF" primer. We then show that this newly designed forward primer combined with the "jgHCO2198" reverse primer to target a 313 bp fragment performs well across metazoan diversity, with higher success rates than versatile primer sets traditionally used for DNA barcoding (i.e. LCO1490/HCO2198). Finally, we demonstrate how the shorter COI fragment coupled with an efficient bioinformatics pipeline can be used to characterize species diversity from environmental samples by pyrosequencing. We examine the gut contents of three species of planktivorous and benthivorous coral reef fish (family: Apogonidae and Holocentridae). After the removal of dubious COI sequences, we obtained a total of 334 prey Operational Taxonomic Units (OTUs) belonging to 14 phyla from 16 fish guts. Of these, 52.5% matched a reference barcode (>98% sequence similarity) and an additional 32% could be assigned to a higher taxonomic level using Bayesian assignment.ConclusionsThe molecular analysis of gut contents targeting the 313 COI fragment using the newly designed mlCOIintF primer in combination with the jgHCO2198 primer offers enormous promise for metazoan metabarcoding studies. We believe that this primer set will be a valuable asset for a range of applications from large-scale biodiversity assessments to food web studies.

Dataset Information

Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents.

Publications

Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents.

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