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Analysis of genomic variation to evaluate the impact of climate changes of the late Quaternary on the species range of a European boreo-montane leaf beetle.

par Sorel, Maeva
Président du jury Noret, Nausicaa
Promoteur Mardulyn, Patrick
Publication Non publié, 2025-11-18

Thèse de doctorat

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Résumé :

Phylogeography integrates population genetics, phylogenetics, and biogeography to understand how historical processes such as glaciations, migrations, and geographic isolation shaped the geographic distribution of genetic lineages within species. Recent advances in bioinformatics and the availability of reference genomes have significantly improved our ability to estimate demographic evolution. Characterizing variation at the level of entire genomes allows us to estimate linkage disequilibrium, a key parameter for demographic inference. At first, whole-genome analyses were computationally demanding and often requiring high-quality phased genomes, limiting the number of individuals included in such studies. More recent tools have become more powerful, allowing to handle more individuals, genetic variants, and complex scenarios. The Quaternary period, particularly the last 800,000 years, has seen intense climatic oscillations that have repeatedly reshaped species' distributions. While temperate species in Europe have been extensively studied in this context, cold-adapted taxa (currently restricted to northern latitudes or southern mountain ranges) have received attention only more recently. Three main hypotheses could explain their glacial survival: expansion into lowlands during glaciations, persistence in peripheral refugia, or survival on nunataks (ice-free mountainpeaks). However, no consensus has been reached, as different species exhibit varying patterns of demographic evolution.This study investigates the demographic history of Gonioctena quinquepunctata, a cold-adapted insect inhabiting mid-altitude habitats (600–1500 m) across several southern European mountain ranges, including the Alps, Massif Central, Pyrenees, and Vosges. Due to its ecological specialization and limited dispersal ability, this species is particularly sensitive to climatic changes, making it a suitable model for testing competing hypotheses of glacial refugia. Using a newly assembled reference genome, RAD-seq data were aligned to assess current genetic variation across the species range. Composite-likelihood analyses rejected the lowland glacial refuge hypothesis in favor of peripheral refugia, contradicting climatic niche modelisation that indicated lowland suitability, a pattern observed in other taxa as well. Demographic reconstructions suggested an initial colonization of the Massif Central from the Alps, followed by postglacial expansion into the Vosges and Pyrenees. Whole-genome sequencing of additional eastern Alpine individuals revealed two genetically distinct lineages (eastern and western), suggesting multiple glacial refugia within the Alps. This was confirmed using Approximate Bayesian Computation and a novel summary statistic, DSVSF (Distribution of Spatial Variation in SNP Frequencies), which outperformed traditional metrics like heterozygosity in distinguishing between evolutionary scenarios, while producing consistent results. Further demographic analysis using SMC++ inferred an ancient colonization of the Vosges from the Alps, Vosges which then colonized the Massif Central and the Pyrenees after the end of the glaciation. The complex demographic history extracted from these results allowed us to compare the detailed demographic dynamic of these populations with key paleoclimatic events. The results suggest that population declines were probably indeed driven by temperature decreases per se, but in addition could have been influenced by the increased frequency and intensity of climatic fluctuations.