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...

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Main Authors: Beverly J. French, Yan Wei Lim, Brian J. Zgliczynski, Robert A. Edwards, Forest Rohwer, Stuart A. Sandin
Format: Article
Language:English
Published: Wiley 2020-04-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.6138
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author Beverly J. French
Yan Wei Lim
Brian J. Zgliczynski
Robert A. Edwards
Forest Rohwer
Stuart A. Sandin
author_facet Beverly J. French
Yan Wei Lim
Brian J. Zgliczynski
Robert A. Edwards
Forest Rohwer
Stuart A. Sandin
author_sort Beverly J. French
collection DOAJ
description 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 Methods A comprehensive review of museum records, the primary literature, and unpublished field survey records was undertaken to determine ranges for four “arc‐eye” hawkfish species in the Paracirrhites species complex and a potential hybrid.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.
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spelling doaj.art-97295cfff40b4943ac96ebddf03ae2a92022-12-21T22:57:40ZengWileyEcology and Evolution2045-77582020-04-011073413342310.1002/ece3.6138Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contentsBeverly J. French0Yan Wei Lim1Brian J. Zgliczynski2Robert A. Edwards3Forest Rohwer4Stuart A. Sandin5Center for Marine Biodiversity and Conservation Scripps Institution of OceanographyUniversity of California San Diego CA USADepartment of Biology San Diego State University San Diego CA USACenter for Marine Biodiversity and Conservation Scripps Institution of OceanographyUniversity of California San Diego CA USADepartment of Biology San Diego State University San Diego CA USADepartment of Biology San Diego State University San Diego CA USACenter for Marine Biodiversity and Conservation Scripps Institution of OceanographyUniversity of California San Diego CA USAAbstract 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.https://doi.org/10.1002/ece3.6138biodiversitycoexistencehawkfishmetagenomicsrare speciestrophic ecology
spellingShingle Beverly J. French
Yan Wei Lim
Brian J. Zgliczynski
Robert A. Edwards
Forest Rohwer
Stuart A. Sandin
Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
Ecology and Evolution
biodiversity
coexistence
hawkfish
metagenomics
rare species
trophic ecology
title Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
title_full Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
title_fullStr Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
title_full_unstemmed Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
title_short Decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
title_sort decoding diversity in a coral reef fish species complex with restricted range using metagenomic sequencing of gut contents
topic biodiversity
coexistence
hawkfish
metagenomics
rare species
trophic ecology
url https://doi.org/10.1002/ece3.6138
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