Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting

Abstract Background Delimiting species across a speciation continuum is a complex task, as the process of species origin is not generally instantaneous. The use of genome-wide data provides unprecedented resolution to address convoluted species delimitation cases, often unraveling cryptic diversity....

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Main Authors: Victor Julio Piñeros, Carmen del R. Pedraza-Marrón, Isaí Betancourt-Resendes, Nancy Calderón-Cortés, Ricardo Betancur-R, Omar Domínguez-Domínguez
Format: Article
Language:English
Published: BMC 2022-09-01
Series:BMC Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1186/s12862-022-02063-0
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author Victor Julio Piñeros
Carmen del R. Pedraza-Marrón
Isaí Betancourt-Resendes
Nancy Calderón-Cortés
Ricardo Betancur-R
Omar Domínguez-Domínguez
author_facet Victor Julio Piñeros
Carmen del R. Pedraza-Marrón
Isaí Betancourt-Resendes
Nancy Calderón-Cortés
Ricardo Betancur-R
Omar Domínguez-Domínguez
author_sort Victor Julio Piñeros
collection DOAJ
description Abstract Background Delimiting species across a speciation continuum is a complex task, as the process of species origin is not generally instantaneous. The use of genome-wide data provides unprecedented resolution to address convoluted species delimitation cases, often unraveling cryptic diversity. However, because genome-wide approaches based on the multispecies coalescent model are known to confound population structure with species boundaries, often resulting in taxonomic over-splitting, it has become increasingly evident that species delimitation research must consider multiple lines of evidence. In this study, we used phylogenomic, population genomic, and coalescent-based species delimitation approaches, and examined those in light of morphological and ecological information, to investigate species numbers and boundaries comprising the Chirostoma “humboltianum group” (family Atherinidae). The humboltianum group is a taxonomically controversial species complex where previous morphological and mitochondrial studies produced conflicting species delimitation outcomes. We generated ddRADseq data for 77 individuals representing the nine nominal species in the group, spanning their distribution range in the central Mexican plateau. Results Our results conflict with the morphospecies and ecological delimitation hypotheses, identifying four independently evolving lineages organized in three geographically cohesive clades: (i) chapalae and sphyraena groups in Lake Chapala, (ii) estor group in Lakes Pátzcuaro and Zirahuén, and (iii) humboltianum sensu stricto group in Lake Zacapu and Lerma river system. Conclusions Overall, our study provides an atypical example where genome-wide analyses delineate fewer species than previously recognized on the basis of morphology. It also highlights the influence of the geological history of the Chapala-Lerma hydrological system in driving allopatric speciation in the humboltianum group.
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spelling doaj.art-66c20ed3ee704f79a8fc177632cfa3d22022-12-22T03:16:40ZengBMCBMC Ecology and Evolution2730-71822022-09-0122111910.1186/s12862-022-02063-0Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splittingVictor Julio Piñeros0Carmen del R. Pedraza-Marrón1Isaí Betancourt-Resendes2Nancy Calderón-Cortés3Ricardo Betancur-R4Omar Domínguez-Domínguez5Laboratorio de Ecología Molecular, Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autónoma de MéxicoDepartment of Biology, The University of OklahomaFacultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de Las Ciencias S/N Juriquilla, Delegación Santa Rosa JáureguiLaboratorio de Ecología Molecular, Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autónoma de MéxicoDepartment of Biology, The University of OklahomaLaboratorio de Biología Acuática, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Edificio “R” Planta BajaAbstract Background Delimiting species across a speciation continuum is a complex task, as the process of species origin is not generally instantaneous. The use of genome-wide data provides unprecedented resolution to address convoluted species delimitation cases, often unraveling cryptic diversity. However, because genome-wide approaches based on the multispecies coalescent model are known to confound population structure with species boundaries, often resulting in taxonomic over-splitting, it has become increasingly evident that species delimitation research must consider multiple lines of evidence. In this study, we used phylogenomic, population genomic, and coalescent-based species delimitation approaches, and examined those in light of morphological and ecological information, to investigate species numbers and boundaries comprising the Chirostoma “humboltianum group” (family Atherinidae). The humboltianum group is a taxonomically controversial species complex where previous morphological and mitochondrial studies produced conflicting species delimitation outcomes. We generated ddRADseq data for 77 individuals representing the nine nominal species in the group, spanning their distribution range in the central Mexican plateau. Results Our results conflict with the morphospecies and ecological delimitation hypotheses, identifying four independently evolving lineages organized in three geographically cohesive clades: (i) chapalae and sphyraena groups in Lake Chapala, (ii) estor group in Lakes Pátzcuaro and Zirahuén, and (iii) humboltianum sensu stricto group in Lake Zacapu and Lerma river system. Conclusions Overall, our study provides an atypical example where genome-wide analyses delineate fewer species than previously recognized on the basis of morphology. It also highlights the influence of the geological history of the Chapala-Lerma hydrological system in driving allopatric speciation in the humboltianum group.https://doi.org/10.1186/s12862-022-02063-0Chirostoma humboldtianumFreshwater fishesGenome-wide dataGenomic structureSNP lociSpecies delimitation
spellingShingle Victor Julio Piñeros
Carmen del R. Pedraza-Marrón
Isaí Betancourt-Resendes
Nancy Calderón-Cortés
Ricardo Betancur-R
Omar Domínguez-Domínguez
Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
BMC Ecology and Evolution
Chirostoma humboldtianum
Freshwater fishes
Genome-wide data
Genomic structure
SNP loci
Species delimitation
title Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
title_full Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
title_fullStr Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
title_full_unstemmed Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
title_short Genome-wide species delimitation analyses of a silverside fish species complex in central Mexico indicate taxonomic over-splitting
title_sort genome wide species delimitation analyses of a silverside fish species complex in central mexico indicate taxonomic over splitting
topic Chirostoma humboldtianum
Freshwater fishes
Genome-wide data
Genomic structure
SNP loci
Species delimitation
url https://doi.org/10.1186/s12862-022-02063-0
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