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Lack of gene flow : Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species

Talla, Venkat ; Johansson, Anna LU ; Dincă, Vlad ; Vila, Roger ; Friberg, Magne LU ; Wiklund, Christer and Backström, Niclas (2019) In Molecular Ecology 28(16). p.3756-3770
Abstract

Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large-scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence-whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole-genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for... (More)

Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large-scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence-whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole-genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)-a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST ) regions generally had low genetic diversity (θπ ), but increased absolute divergence (DXY ) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.

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author
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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Animals, Asia, Bacterial Proteins, Butterflies/classification, DNA, Mitochondrial/genetics, Europe, Gene Flow, Gene Frequency, Genetic Speciation, Genetic Variation, Genetics, Population, Genome, Repressor Proteins, Selection, Genetic, Whole Genome Sequencing
in
Molecular Ecology
volume
28
issue
16
pages
3756 - 3770
publisher
Wiley-Blackwell
external identifiers
  • scopus:85070695240
  • pmid:31325366
ISSN
0962-1083
DOI
10.1111/mec.15188
language
English
LU publication?
yes
additional info
© 2019 John Wiley & Sons Ltd.
id
a11e7ce0-54d9-479d-8567-144f408764e1
date added to LUP
2021-01-28 13:26:48
date last changed
2024-03-21 01:38:59
@article{a11e7ce0-54d9-479d-8567-144f408764e1,
  abstract     = {{<p>Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large-scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence-whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole-genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)-a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST ) regions generally had low genetic diversity (θπ ), but increased absolute divergence (DXY ) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.</p>}},
  author       = {{Talla, Venkat and Johansson, Anna and Dincă, Vlad and Vila, Roger and Friberg, Magne and Wiklund, Christer and Backström, Niclas}},
  issn         = {{0962-1083}},
  keywords     = {{Animals; Asia; Bacterial Proteins; Butterflies/classification; DNA, Mitochondrial/genetics; Europe; Gene Flow; Gene Frequency; Genetic Speciation; Genetic Variation; Genetics, Population; Genome; Repressor Proteins; Selection, Genetic; Whole Genome Sequencing}},
  language     = {{eng}},
  number       = {{16}},
  pages        = {{3756--3770}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Molecular Ecology}},
  title        = {{Lack of gene flow : Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species}},
  url          = {{http://dx.doi.org/10.1111/mec.15188}},
  doi          = {{10.1111/mec.15188}},
  volume       = {{28}},
  year         = {{2019}},
}