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Mapping species birth across the recombination landscapes of marine snails
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  • Emily Giles,
  • Romuald Laso-Jadart,
  • Daniel Ortiz-Barrientos,
  • Paulina Carimán,
  • Erwan Delrieu-Trottin,
  • Marie-Laure Guillemin,
  • Stefano Mona,
  • Xavier Pochon,
  • Pablo Saenz-Agudelo
Emily Giles
Universidad Austral de Chile

Corresponding Author:emily.c.giles@gmail.com

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Romuald Laso-Jadart
Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, EPHE-PSL, Université PSL, CNRS, SU, UA
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Daniel Ortiz-Barrientos
The University of Queenland
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Paulina Carimán
El Instituto de Ciencias Ambientales y Evolutivas
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Erwan Delrieu-Trottin
Université Montpellier
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Marie-Laure Guillemin
Universidad Austral de Chile
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Stefano Mona
Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, EPHE-PSL, Université PSL, CNRS, SU, UA
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Xavier Pochon
Cawthron Institute
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Pablo Saenz-Agudelo
Universidad Austral de Chile
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Abstract

Understanding the drivers of heterogenous genomic divergence is essential for uncovering the mechanisms that generate and constrain biodiversity. The extent to which adaptation and speciation are facilitated by reorganization of the recombination landscape remains untested in many systems. Marine ecosystems, with their dynamic and fluid habitats, offer a compelling context to investigate genomic divergence. In this study we mapped genomic divergence and selection across recombination landscapes of parapatric marine snail sister species that we show have recently undergone secondary contact. Regions of reduced recombination were enriched for genes exhibiting signatures of negative selection, whereas regions of high recombination were associated with genes under putative positive selection. Notably, the recombination landscape of the population in parapatry of one species (Scurria viridula) differs markedly from that of the other population within this same species, highlighting the role of introgression in reshaping recombination landscapes. In the other species (Scurria zebrina), conservation of the recombination landscape and divergent selection among populations suggest trapping of beneficial allele combinations in regions of low recombination maintain the identity of this species. Among species, signals of divergence with gene flow consistently cluster within specific genomic regions characterized by high recombination rate variation among the populations of S. viridula. These results challenge theoretical expectations of recombination evolution by showing that the causes of genomic divergence can be population- specific. This study demonstrates that recombination landscapes are key modulators of genomic divergence, with contemporary evolutionary shifts that could enable populations to adapt to distinct environments. Our findings provide new insights into the interplay between recombination, selection, and gene flow during speciation, underscoring the complexity of evolutionary trajectories in marine systems.