ORCID

Abstract

An intricate interplay between evolutionary and demographic processes has frequently resulted in complex patterns of genetic and phenotypic diversity in alpine lineages, posing serious challenges to species delimitation and biodiversity conservation planning. Here we integrate genomic data, geometric morphometric analyses and thermal tolerance experiments to explore the role of Pleistocene climatic changes and adaptation to alpine environments on patterns of genomic and phenotypic variation in diving beetles from the taxonomically complex Agabus bipustulatus species group. Genetic structure and phylogenomic analyses revealed the presence of three geographically cohesive lineages, two representing trans-Palearctic and Iberian populations of the elevation-generalist A. bipustulatus and another corresponding to the strictly-alpine A. nevadensis, a narrow-range endemic taxon from the Sierra Nevada mountain range in southeastern Iberia. The best-supported model of lineage divergence, along with the existence of pervasive genetic introgression and admixture in secondary contact zones, is consistent with a scenario of population isolation and connectivity linked to Quaternary climatic oscillations. Our results suggest that A. nevadensis is an alpine ecotype of A. bipustulatus, whose genotypic, morphological and physiological differentiation likely resulted from an interplay between population isolation and local altitudinal adaptation. Remarkably, within the Iberian Peninsula, such ecotypic differentiation is unique to Sierra Nevada populations and has not been replicated in other alpine populations of A. bipustulatus. Collectively, our study supports fast ecotypic differentiation and incipient speciation processes within the study complex and points to Pleistocene glaciations and local adaptation along elevational gradients as key drivers of biodiversity generation in alpine environments.

Publication Date

2024-08-07

Publication Title

Molecular Ecology

Volume

33

Issue

17

ISSN

0962-1083

Acceptance Date

2024-07-22

Deposit Date

2024-07-23

Funding

This work was supported by the R&D project id. PID2019\u2010108895GB\u2010I00, funded by MCIN/AEI/ 10.13039/501100011033 and VI PPIT Universidad de Sevilla (IV.7 Ayuda Suplementaria a Grupos de Investigaci\u00F3n por captaci\u00F3n de fondos en las convocatorias de proyectos de investigaci\u00F3n del Plan Estatal; 2020/1110). Logistic support was provided by Laboratorio de Ecolog\u00EDa Molecular (LEM\u2010EBD) from Estaci\u00F3n Biol\u00F3gica de Do\u00F1ana (CSIC). We also thank Centro de Supercomputaci\u00F3n de Galicia (CESGA) and Do\u00F1ana's Singular Scientific\u2010Technical Infrastructure (ICTS\u2010RBD) for access to computer resources. SP is funded by a postdoctoral contract from the \u2018Consejer\u00EDa de Econom\u00EDa, Conocimiento, Empresas y Universidad de la Junta de Andaluc\u00EDa\u2010Fondo Social Europeo de Andaluc\u00EDa 2014\u20102020\u2019 (\u2018Talento Doctores, PID 2020\u2019 program, grant id. SP\u2010DOC_01211). JAC is funded by a postdoctoral contract from the \u2018Mar\u00EDa Zambrano\u2019 program (grant id. 19868), by the Spanish \u2018Ministerio de Universidades\u2019 (funded by European Union \u2013 NextGenerationEU). The Sierra Nevada National Park authorities and Andalusian Government provided logistic help and sampling permissions. We are especially grateful to F\u00E9lix Picazo, David S\u00E1nchez\u2010Fern\u00E1ndez and Narcisa Mart\u00EDnez for help at various stages of this project. DTB thanks Rebecca Bilton, Shidi and Fara Hosseinie, Hiva Nasserzadeh, Michael Balke, Mario Toledo, Antonio Schizzerotto and Steven Routledge for their help in the field. We thank three anonymous referees for their constructive and valuable comments on an earlier version of the manuscript.

Keywords

Coleoptera, Pleistocene speciation, alpine ecosystems, glacial refugia, hybridisation, integrative taxonomy, sky-islands

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