A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris

Mitochondrial DNA (mtDNA) sequencing has led to an unprecedented rise in the identification of cryptic species. However, it is widely acknowledged that nuclear DNA (nuDNA) sequence data are also necessary to properly define species boundaries. Next generation sequencing techniques provide a wealth of nuclear genomic data, which can be used to ascertain both the evolutionary history and taxonomic status of putative cryptic species. Here, we focus on the intriguing case of the butterfly Thymelicus sylvestris (Lepidoptera: Hesperiidae). We identified six deeply diverged mitochondrial lineages; three distributed all across Europe and found in sympatry, suggesting a potential case of cryptic species. We then sequenced these six lineages using double‐digest restriction‐site associated DNA sequencing (ddRADseq). Nuclear genomic loci contradicted mtDNA patterns and genotypes generally clustered according to geography, i.e., a pattern expected under the assumption of postglacial recolonization from different refugia. Further analyses indicated that this strong mtDNA/nuDNA discrepancy cannot be explained by incomplete lineage sorting, sex‐biased asymmetries, NUMTs, natural selection, introgression or Wolbachia‐mediated genetic sweeps. We suggest that this mitonuclear discordance was caused by long periods of geographic isolation followed by range expansions, homogenizing the nuclear but not the mitochondrial genome. These results highlight T. sylvestris as a potential case of multiple despeciation and/or lineage fusion events. We finally argue, since mtDNA and nuDNA do not necessarily follow the same mechanisms of evolution, their respective evolutionary history reflects complementary aspects of past demographic and biogeographic events.

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Main Authors: Hinojosa, Joan Carles, Koubínová, Darina, Szenteczki, Mark A., Pitteloud, Camille, Dincă, Vlad, Álvarez, Nadir, Vila, Roger
Other Authors: Ministerio de Economía y Competitividad (España)
Format: artículo biblioteca
Language:English
Published: Wiley-Blackwell 2019-09
Subjects:Despeciation, Genomics, Lepidoptera, Lineage fusion, Mitochondrial DNA, RAD sequencing,
Online Access:http://hdl.handle.net/10261/202320
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/501100003329
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spelling dig-ibe-es-10261-2023202020-10-13T09:14:37Z A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris Hinojosa, Joan Carles Koubínová, Darina Szenteczki, Mark A. Pitteloud, Camille Dincă, Vlad Álvarez, Nadir Vila, Roger Ministerio de Economía y Competitividad (España) European Commission Generalitat de Catalunya Swiss National Science Foundation Ministry of Education, Youth and Sports (Czech Republic) CERIT Scientific Cloud (Czech Republic) Hinojosa, Joan Carles [0000-0002-6318-4252] Koubínová, Darina [0000-0002-1854-7675] Szenteczki, Mark A. [0000-0002-3049-8327] Alvarez, Nadir [0000-0002-0729-166X] Vila, Roger [0000-0002-2447-4388] Despeciation Genomics Lepidoptera Lineage fusion Mitochondrial DNA RAD sequencing Mitochondrial DNA (mtDNA) sequencing has led to an unprecedented rise in the identification of cryptic species. However, it is widely acknowledged that nuclear DNA (nuDNA) sequence data are also necessary to properly define species boundaries. Next generation sequencing techniques provide a wealth of nuclear genomic data, which can be used to ascertain both the evolutionary history and taxonomic status of putative cryptic species. Here, we focus on the intriguing case of the butterfly Thymelicus sylvestris (Lepidoptera: Hesperiidae). We identified six deeply diverged mitochondrial lineages; three distributed all across Europe and found in sympatry, suggesting a potential case of cryptic species. We then sequenced these six lineages using double‐digest restriction‐site associated DNA sequencing (ddRADseq). Nuclear genomic loci contradicted mtDNA patterns and genotypes generally clustered according to geography, i.e., a pattern expected under the assumption of postglacial recolonization from different refugia. Further analyses indicated that this strong mtDNA/nuDNA discrepancy cannot be explained by incomplete lineage sorting, sex‐biased asymmetries, NUMTs, natural selection, introgression or Wolbachia‐mediated genetic sweeps. We suggest that this mitonuclear discordance was caused by long periods of geographic isolation followed by range expansions, homogenizing the nuclear but not the mitochondrial genome. These results highlight T. sylvestris as a potential case of multiple despeciation and/or lineage fusion events. We finally argue, since mtDNA and nuDNA do not necessarily follow the same mechanisms of evolution, their respective evolutionary history reflects complementary aspects of past demographic and biogeographic events. Financial support for this research was provided by project CGL2016‐76322‐P (AEI/FEDER, UE) and 2017‐SGR‐991 (Generalitat de Catalunya) to Roger Vila and by predoctoral fellowship BES‐2017‐080641 to Joan Carles Hinojosa. Nadir Alvarez was funded by project PP00P3_172899 from the Swiss National Science Foundation. Computational resources for certain analyses were supplied by the Ministry of Education, Youth and Sports of the Czech Republic under the Projects CESNET (Project No. LM2015042) and CERIT‐Scientific Cloud (Project No. LM2015085) provided within the program Projects of Large Research, Development and Innovations Infrastructures. Peer reviewed 2020-03-02T08:43:47Z 2020-03-02T08:43:47Z 2019-09 artículo http://purl.org/coar/resource_type/c_6501 Molecular Ecology 28(17): 3857-3868 (2019) 0962-1083 http://hdl.handle.net/10261/202320 10.1111/mec.15153 1365-294X http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100002809 http://dx.doi.org/10.13039/501100003329 en #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2016-76322-P Postprint https://doi.org/10.1111/mec.15153 Sí open Wiley-Blackwell
institution IBE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ibe-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IBE España
language English
topic Despeciation
Genomics
Lepidoptera
Lineage fusion
Mitochondrial DNA
RAD sequencing
Despeciation
Genomics
Lepidoptera
Lineage fusion
Mitochondrial DNA
RAD sequencing
spellingShingle Despeciation
Genomics
Lepidoptera
Lineage fusion
Mitochondrial DNA
RAD sequencing
Despeciation
Genomics
Lepidoptera
Lineage fusion
Mitochondrial DNA
RAD sequencing
Hinojosa, Joan Carles
Koubínová, Darina
Szenteczki, Mark A.
Pitteloud, Camille
Dincă, Vlad
Álvarez, Nadir
Vila, Roger
A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
description Mitochondrial DNA (mtDNA) sequencing has led to an unprecedented rise in the identification of cryptic species. However, it is widely acknowledged that nuclear DNA (nuDNA) sequence data are also necessary to properly define species boundaries. Next generation sequencing techniques provide a wealth of nuclear genomic data, which can be used to ascertain both the evolutionary history and taxonomic status of putative cryptic species. Here, we focus on the intriguing case of the butterfly Thymelicus sylvestris (Lepidoptera: Hesperiidae). We identified six deeply diverged mitochondrial lineages; three distributed all across Europe and found in sympatry, suggesting a potential case of cryptic species. We then sequenced these six lineages using double‐digest restriction‐site associated DNA sequencing (ddRADseq). Nuclear genomic loci contradicted mtDNA patterns and genotypes generally clustered according to geography, i.e., a pattern expected under the assumption of postglacial recolonization from different refugia. Further analyses indicated that this strong mtDNA/nuDNA discrepancy cannot be explained by incomplete lineage sorting, sex‐biased asymmetries, NUMTs, natural selection, introgression or Wolbachia‐mediated genetic sweeps. We suggest that this mitonuclear discordance was caused by long periods of geographic isolation followed by range expansions, homogenizing the nuclear but not the mitochondrial genome. These results highlight T. sylvestris as a potential case of multiple despeciation and/or lineage fusion events. We finally argue, since mtDNA and nuDNA do not necessarily follow the same mechanisms of evolution, their respective evolutionary history reflects complementary aspects of past demographic and biogeographic events.
author2 Ministerio de Economía y Competitividad (España)
author_facet Ministerio de Economía y Competitividad (España)
Hinojosa, Joan Carles
Koubínová, Darina
Szenteczki, Mark A.
Pitteloud, Camille
Dincă, Vlad
Álvarez, Nadir
Vila, Roger
format artículo
topic_facet Despeciation
Genomics
Lepidoptera
Lineage fusion
Mitochondrial DNA
RAD sequencing
author Hinojosa, Joan Carles
Koubínová, Darina
Szenteczki, Mark A.
Pitteloud, Camille
Dincă, Vlad
Álvarez, Nadir
Vila, Roger
author_sort Hinojosa, Joan Carles
title A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
title_short A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
title_full A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
title_fullStr A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
title_full_unstemmed A mirage of cryptic species: Genomics uncover striking mitonuclear discordance in the butterfly Thymelicus sylvestris
title_sort mirage of cryptic species: genomics uncover striking mitonuclear discordance in the butterfly thymelicus sylvestris
publisher Wiley-Blackwell
publishDate 2019-09
url http://hdl.handle.net/10261/202320
http://dx.doi.org/10.13039/501100000780
http://dx.doi.org/10.13039/501100002809
http://dx.doi.org/10.13039/501100003329
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