---
OA_place: publisher
OA_type: gold
_id: '18908'
abstract:
- lang: eng
  text: Chromosomal rearrangements can lead to the coupling of reproductive barriers,
    but whether and how they contribute to the completion of speciation remains unclear.
    Marine snails of the genus Littorina repeatedly form hybrid zones between populations
    segregating for multiple inversion arrangements, providing opportunities to study
    their barrier effects. Here, we analyzed 2 adjacent transects across hybrid zones
    between 2 ecotypes of Littorina fabalis (“large” and “dwarf”) adapted to different
    wave exposure conditions on a Swedish island. Applying whole-genome sequencing,
    we found 12 putative inversions on 9 of 17 chromosomes. Nine of the putative inversions
    reached near differential fixation between the 2 ecotypes, and all were in strong
    linkage disequilibrium. These inversions cover 20% of the genome and carry 93%
    of divergent single nucleotide polymorphisms (SNPs). Bimodal hybrid zones in both
    transects indicated that the 2 ecotypes of Littorina fabalis maintain their genetic
    and phenotypic integrity following contact. The bimodality reflects the strong
    coupling between inversion clines and the extension of the barrier effect across
    the whole genome. Demographic inference suggests that coupling arose during a
    period of allopatry and has been maintained for > 1,000 generations after
    secondary contact. Overall, this study shows that the coupling of multiple chromosomal
    inversions contributes to strong reproductive isolation. Notably, 2 of the putative
    inversions overlap with inverted genomic regions associated with ecotype differences
    in a closely related species (Littorina saxatilis), suggesting the same regions,
    with similar structural variants, repeatedly contribute to ecotype evolution in
    distinct species.
acknowledgement: The computations and data handling were enabled by resources provided
  by the Swedish National Infrastructure for Computing at UPPMAX partially funded
  by the Swedish Research Council through grant agreement no. 2018-05973. We thank
  all the member of the Littorina team for the stimulating discussions about the manuscripts,
  James Reeves for his help the implementation of Hsplit, and Thomas Broquet for his
  useful comments in the latter stage of manuscript revisions.
article_processing_charge: Yes
article_type: letter_note
author:
- first_name: Alan
  full_name: Le Moan, Alan
  last_name: Le Moan
- first_name: Sean
  full_name: Stankowski, Sean
  id: 43161670-5719-11EA-8025-FABC3DDC885E
  last_name: Stankowski
- first_name: Marina
  full_name: Rafajlović, Marina
  last_name: Rafajlović
- first_name: Olga
  full_name: Ortega-Martinez, Olga
  last_name: Ortega-Martinez
- first_name: Rui
  full_name: Faria, Rui
  last_name: Faria
- first_name: Roger K
  full_name: Butlin, Roger K
  last_name: Butlin
- first_name: Kerstin
  full_name: Johannesson, Kerstin
  last_name: Johannesson
citation:
  ama: Le Moan A, Stankowski S, Rafajlović M, et al. Coupling of twelve putative chromosomal
    inversions maintains a strong barrier to gene flow between snail ecotypes. <i>Evolution
    Letters</i>. 2024;8(4):575-586. doi:<a href="https://doi.org/10.1093/evlett/qrae014">10.1093/evlett/qrae014</a>
  apa: Le Moan, A., Stankowski, S., Rafajlović, M., Ortega-Martinez, O., Faria, R.,
    Butlin, R. K., &#38; Johannesson, K. (2024). Coupling of twelve putative chromosomal
    inversions maintains a strong barrier to gene flow between snail ecotypes. <i>Evolution
    Letters</i>. Oxford University Press. <a href="https://doi.org/10.1093/evlett/qrae014">https://doi.org/10.1093/evlett/qrae014</a>
  chicago: Le Moan, Alan, Sean Stankowski, Marina Rafajlović, Olga Ortega-Martinez,
    Rui Faria, Roger K Butlin, and Kerstin Johannesson. “Coupling of Twelve Putative
    Chromosomal Inversions Maintains a Strong Barrier to Gene Flow between Snail Ecotypes.”
    <i>Evolution Letters</i>. Oxford University Press, 2024. <a href="https://doi.org/10.1093/evlett/qrae014">https://doi.org/10.1093/evlett/qrae014</a>.
  ieee: A. Le Moan <i>et al.</i>, “Coupling of twelve putative chromosomal inversions
    maintains a strong barrier to gene flow between snail ecotypes,” <i>Evolution
    Letters</i>, vol. 8, no. 4. Oxford University Press, pp. 575–586, 2024.
  ista: Le Moan A, Stankowski S, Rafajlović M, Ortega-Martinez O, Faria R, Butlin
    RK, Johannesson K. 2024. Coupling of twelve putative chromosomal inversions maintains
    a strong barrier to gene flow between snail ecotypes. Evolution Letters. 8(4),
    575–586.
  mla: Le Moan, Alan, et al. “Coupling of Twelve Putative Chromosomal Inversions Maintains
    a Strong Barrier to Gene Flow between Snail Ecotypes.” <i>Evolution Letters</i>,
    vol. 8, no. 4, Oxford University Press, 2024, pp. 575–86, doi:<a href="https://doi.org/10.1093/evlett/qrae014">10.1093/evlett/qrae014</a>.
  short: A. Le Moan, S. Stankowski, M. Rafajlović, O. Ortega-Martinez, R. Faria, R.K.
    Butlin, K. Johannesson, Evolution Letters 8 (2024) 575–586.
date_created: 2025-01-27T13:30:27Z
date_published: 2024-04-23T00:00:00Z
date_updated: 2025-09-09T12:05:51Z
day: '23'
ddc:
- '570'
department:
- _id: NiBa
doi: 10.1093/evlett/qrae014
external_id:
  isi:
  - '001206532900001'
  pmid:
  - '39479507'
file:
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  creator: dernst
  date_created: 2025-01-27T13:33:14Z
  date_updated: 2025-01-27T13:33:14Z
  file_id: '18909'
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  relation: main_file
  success: 1
file_date_updated: 2025-01-27T13:33:14Z
has_accepted_license: '1'
intvolume: '         8'
isi: 1
issue: '4'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc/4.0/
month: '04'
oa: 1
oa_version: Published Version
page: 575-586
pmid: 1
publication: Evolution Letters
publication_identifier:
  issn:
  - 2056-3744
publication_status: published
publisher: Oxford University Press
quality_controlled: '1'
scopus_import: '1'
status: public
title: Coupling of twelve putative chromosomal inversions maintains a strong barrier
  to gene flow between snail ecotypes
tmp:
  image: /images/cc_by_nc.png
  legal_code_url: https://creativecommons.org/licenses/by-nc/4.0/legalcode
  name: Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
  short: CC BY-NC (4.0)
type: journal_article
user_id: 317138e5-6ab7-11ef-aa6d-ffef3953e345
volume: 8
year: '2024'
...
---
_id: '12521'
abstract:
- lang: eng
  text: Differentiated X chromosomes are expected to have higher rates of adaptive
    divergence than autosomes, if new beneficial mutations are recessive (the “faster-X
    effect”), largely because these mutations are immediately exposed to selection
    in males. The evolution of X chromosomes after they stop recombining in males,
    but before they become hemizygous, has not been well explored theoretically. We
    use the diffusion approximation to infer substitution rates of beneficial and
    deleterious mutations under such a scenario. Our results show that selection is
    less efficient on diploid X loci than on autosomal and hemizygous X loci under
    a wide range of parameters. This “slower-X” effect is stronger for genes affecting
    primarily (or only) male fitness, and for sexually antagonistic genes. These unusual
    dynamics suggest that some of the peculiar features of X chromosomes, such as
    the differential accumulation of genes with sex-specific functions, may start
    arising earlier than previously appreciated.
acknowledgement: We thank the Vicoso and Barton groups and ISTA Scientific Computing
  Unit. We also thank two anonymous reviewers for their valuable comments. This work
  was supported by the European Research Council under the European Union’s Horizon
  2020 research and innovation program (grant agreements no. 715257 and no. 716117).
article_number: qrac004
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Andrea
  full_name: Mrnjavac, Andrea
  id: 353FAC84-AE61-11E9-8BFC-00D3E5697425
  last_name: Mrnjavac
- first_name: Kseniia
  full_name: Khudiakova, Kseniia
  id: 4E6DC800-AE37-11E9-AC72-31CAE5697425
  last_name: Khudiakova
  orcid: 0000-0002-6246-1465
- first_name: Nicholas H
  full_name: Barton, Nicholas H
  id: 4880FE40-F248-11E8-B48F-1D18A9856A87
  last_name: Barton
  orcid: 0000-0002-8548-5240
- first_name: Beatriz
  full_name: Vicoso, Beatriz
  id: 49E1C5C6-F248-11E8-B48F-1D18A9856A87
  last_name: Vicoso
  orcid: 0000-0002-4579-8306
citation:
  ama: 'Mrnjavac A, Khudiakova K, Barton NH, Vicoso B. Slower-X: Reduced efficiency
    of selection in the early stages of X chromosome evolution. <i>Evolution Letters</i>.
    2023;7(1). doi:<a href="https://doi.org/10.1093/evlett/qrac004">10.1093/evlett/qrac004</a>'
  apa: 'Mrnjavac, A., Khudiakova, K., Barton, N. H., &#38; Vicoso, B. (2023). Slower-X:
    Reduced efficiency of selection in the early stages of X chromosome evolution.
    <i>Evolution Letters</i>. Oxford University Press. <a href="https://doi.org/10.1093/evlett/qrac004">https://doi.org/10.1093/evlett/qrac004</a>'
  chicago: 'Mrnjavac, Andrea, Kseniia Khudiakova, Nicholas H Barton, and Beatriz Vicoso.
    “Slower-X: Reduced Efficiency of Selection in the Early Stages of X Chromosome
    Evolution.” <i>Evolution Letters</i>. Oxford University Press, 2023. <a href="https://doi.org/10.1093/evlett/qrac004">https://doi.org/10.1093/evlett/qrac004</a>.'
  ieee: 'A. Mrnjavac, K. Khudiakova, N. H. Barton, and B. Vicoso, “Slower-X: Reduced
    efficiency of selection in the early stages of X chromosome evolution,” <i>Evolution
    Letters</i>, vol. 7, no. 1. Oxford University Press, 2023.'
  ista: 'Mrnjavac A, Khudiakova K, Barton NH, Vicoso B. 2023. Slower-X: Reduced efficiency
    of selection in the early stages of X chromosome evolution. Evolution Letters.
    7(1), qrac004.'
  mla: 'Mrnjavac, Andrea, et al. “Slower-X: Reduced Efficiency of Selection in the
    Early Stages of X Chromosome Evolution.” <i>Evolution Letters</i>, vol. 7, no.
    1, qrac004, Oxford University Press, 2023, doi:<a href="https://doi.org/10.1093/evlett/qrac004">10.1093/evlett/qrac004</a>.'
  short: A. Mrnjavac, K. Khudiakova, N.H. Barton, B. Vicoso, Evolution Letters 7 (2023).
corr_author: '1'
date_created: 2023-02-06T13:59:12Z
date_published: 2023-02-01T00:00:00Z
date_updated: 2026-05-17T22:30:30Z
day: '01'
ddc:
- '570'
department:
- _id: GradSch
- _id: BeVi
doi: 10.1093/evlett/qrac004
ec_funded: 1
external_id:
  isi:
  - '001021692200001'
  pmid:
  - '37065438'
file:
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  checksum: a240a041cb9b9b7c8ba93a4706674a3f
  content_type: application/pdf
  creator: dernst
  date_created: 2023-08-16T11:43:33Z
  date_updated: 2023-08-16T11:43:33Z
  file_id: '14068'
  file_name: 2023_EvLetters_Mrnjavac.pdf
  file_size: 2592189
  relation: main_file
  success: 1
file_date_updated: 2023-08-16T11:43:33Z
has_accepted_license: '1'
intvolume: '         7'
isi: 1
issue: '1'
keyword:
- Genetics
- Ecology
- Evolution
- Behavior and Systematics
language:
- iso: eng
license: https://creativecommons.org/licenses/by/4.0/
month: '02'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 256E75B8-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '716117'
  name: Optimal Transport and Stochastic Dynamics
- _id: 250BDE62-B435-11E9-9278-68D0E5697425
  call_identifier: H2020
  grant_number: '715257'
  name: Prevalence and Influence of Sexual Antagonism on Genome Evolution
publication: Evolution Letters
publication_identifier:
  issn:
  - 2056-3744
publication_status: published
publisher: Oxford University Press
quality_controlled: '1'
related_material:
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  - id: '18531'
    relation: dissertation_contains
    status: public
scopus_import: '1'
status: public
title: 'Slower-X: Reduced efficiency of selection in the early stages of X chromosome
  evolution'
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 7
year: '2023'
...
---
_id: '9917'
abstract:
- lang: eng
  text: Adaptive divergence and speciation may happen despite opposition by gene flow.
    Identifying the genomic basis underlying divergence with gene flow is a major
    task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on
    genomic regions of high differentiation. However, not all genomic architectures
    potentially underlying divergence are expected to show extreme differentiation.
    Here, we develop an approach that combines hybrid zone analysis (i.e., focuses
    on spatial patterns of allele frequency change) with system-specific simulations
    to identify loci inconsistent with neutral evolution. We apply this to a genome-wide
    SNP set from an ideally suited study organism, the intertidal snail Littorina
    saxatilis, which shows primary divergence between ecotypes associated with different
    shore habitats. We detect many SNPs with clinal patterns, most of which are consistent
    with neutrality. Among non-neutral SNPs, most are located within three large putative
    inversions differentiating ecotypes. Many non-neutral SNPs show relatively low
    levels of differentiation. We discuss potential reasons for this pattern, including
    loose linkage to selected variants, polygenic adaptation and a component of balancing
    selection within populations (which may be expected for inversions). Our work
    is in line with theory predicting a role for inversions in divergence, and emphasizes
    that genomic regions contributing to divergence may not always be accessible with
    methods purely based on allele frequency differences. These conclusions call for
    approaches that take spatial patterns of allele frequency change into account
    in other systems.
acknowledgement: We are very grateful to people who helped with fieldwork, snail processing,
  and DNA extractions, particularly Laura Brettell, Mårten Duvetorp, Juan Galindo,
  Anne-Lise Liabot and Irena Senčić. We would also like to thank Magnus Alm Rosenblad
  and Mats Töpel for their contribution to assembling the Littorina saxatilis genome,
  Carl André, Pasi Rastas, and Romain Villoutreix for discussion, and two anonymous
  reviewers for their helpful comments on the manuscript. We are grateful to RapidGenomics
  for library preparation and sequencing. We thank the Natural Environment Research
  Council, the European Research Council and the Swedish Research Councils VR and
  Formas (Linnaeus grant to the Centre for Marine Evolutionary Biology and Tage Erlander
  Guest Professorship) for funding. P.C. was funded by the University of Sheffield
  Vice-chancellor's India scholarship. R.F. is funded by the European Union's Horizon
  2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement
  no. 706376. M. Raf. was supported by the Adlerbert Research Foundation.
article_processing_charge: Yes
article_type: letter_note
author:
- first_name: Anja M
  full_name: Westram, Anja M
  id: 3C147470-F248-11E8-B48F-1D18A9856A87
  last_name: Westram
  orcid: 0000-0003-1050-4969
- first_name: Marina
  full_name: Rafajlović, Marina
  last_name: Rafajlović
- first_name: Pragya
  full_name: Chaube, Pragya
  last_name: Chaube
- first_name: Rui
  full_name: Faria, Rui
  last_name: Faria
- first_name: Tomas
  full_name: Larsson, Tomas
  last_name: Larsson
- first_name: Marina
  full_name: Panova, Marina
  last_name: Panova
- first_name: Mark
  full_name: Ravinet, Mark
  last_name: Ravinet
- first_name: Anders
  full_name: Blomberg, Anders
  last_name: Blomberg
- first_name: Bernhard
  full_name: Mehlig, Bernhard
  last_name: Mehlig
- first_name: Kerstin
  full_name: Johannesson, Kerstin
  last_name: Johannesson
- first_name: Roger
  full_name: Butlin, Roger
  last_name: Butlin
citation:
  ama: 'Westram AM, Rafajlović M, Chaube P, et al. Clines on the seashore: The genomic
    architecture underlying rapid divergence in the face of gene flow. <i>Evolution
    Letters</i>. 2018;2(4):297-309. doi:<a href="https://doi.org/10.1002/evl3.74">10.1002/evl3.74</a>'
  apa: 'Westram, A. M., Rafajlović, M., Chaube, P., Faria, R., Larsson, T., Panova,
    M., … Butlin, R. (2018). Clines on the seashore: The genomic architecture underlying
    rapid divergence in the face of gene flow. <i>Evolution Letters</i>. Wiley. <a
    href="https://doi.org/10.1002/evl3.74">https://doi.org/10.1002/evl3.74</a>'
  chicago: 'Westram, Anja M, Marina Rafajlović, Pragya Chaube, Rui Faria, Tomas Larsson,
    Marina Panova, Mark Ravinet, et al. “Clines on the Seashore: The Genomic Architecture
    Underlying Rapid Divergence in the Face of Gene Flow.” <i>Evolution Letters</i>.
    Wiley, 2018. <a href="https://doi.org/10.1002/evl3.74">https://doi.org/10.1002/evl3.74</a>.'
  ieee: 'A. M. Westram <i>et al.</i>, “Clines on the seashore: The genomic architecture
    underlying rapid divergence in the face of gene flow,” <i>Evolution Letters</i>,
    vol. 2, no. 4. Wiley, pp. 297–309, 2018.'
  ista: 'Westram AM, Rafajlović M, Chaube P, Faria R, Larsson T, Panova M, Ravinet
    M, Blomberg A, Mehlig B, Johannesson K, Butlin R. 2018. Clines on the seashore:
    The genomic architecture underlying rapid divergence in the face of gene flow.
    Evolution Letters. 2(4), 297–309.'
  mla: 'Westram, Anja M., et al. “Clines on the Seashore: The Genomic Architecture
    Underlying Rapid Divergence in the Face of Gene Flow.” <i>Evolution Letters</i>,
    vol. 2, no. 4, Wiley, 2018, pp. 297–309, doi:<a href="https://doi.org/10.1002/evl3.74">10.1002/evl3.74</a>.'
  short: A.M. Westram, M. Rafajlović, P. Chaube, R. Faria, T. Larsson, M. Panova,
    M. Ravinet, A. Blomberg, B. Mehlig, K. Johannesson, R. Butlin, Evolution Letters
    2 (2018) 297–309.
date_created: 2021-08-16T07:45:38Z
date_published: 2018-08-20T00:00:00Z
date_updated: 2024-10-21T06:02:42Z
day: '20'
ddc:
- '570'
department:
- _id: BeVi
doi: 10.1002/evl3.74
external_id:
  isi:
  - '000446774400004'
  pmid:
  - '30283683'
file:
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  creator: asandaue
  date_created: 2021-08-16T07:48:03Z
  date_updated: 2021-08-16T07:48:03Z
  file_id: '9918'
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  success: 1
file_date_updated: 2021-08-16T07:48:03Z
has_accepted_license: '1'
intvolume: '         2'
isi: 1
issue: '4'
language:
- iso: eng
month: '08'
oa: 1
oa_version: Published Version
page: 297-309
pmid: 1
publication: Evolution Letters
publication_identifier:
  eissn:
  - 2056-3744
  issn:
  - 2056-3744
publication_status: published
publisher: Wiley
quality_controlled: '1'
related_material:
  record:
  - id: '9930'
    relation: research_data
    status: public
scopus_import: '1'
status: public
title: 'Clines on the seashore: The genomic architecture underlying rapid divergence
  in the face of gene flow'
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 2
year: '2018'
...