Embracing genomic incongruence: the evolutionary forces shaping the white oak species complex in Southeastern Europe
(2) Transilvania University of Brașov, Brașov, Romania
(3) University of Forestry, Sofia, Bulgaria
(4) Institute of Bioscience and Bioresources (IBBR), National Research Council (CNR), Firenze, Italy
(5) National Botanical Garden of Georgia, Tbilisi, Georgia
(6) Hungarian Institute of Agriculture and Life Sciences (MATE), Hungary
(7) National Botanical Garden of Türkiye (NBGT) / TAGEM, Türkiye
(8) Middle East Technical University (METU), Türkiye
(9) Aristotle University of Thessaloniki, Thessaloniki, Greece
(10) Swiss Federal Research Institute WSL, Birmensdorf, Switzerland
Abstract
Defining species boundaries in complex evolutionary systems remains a major challenge in taxonomy. White oaks (Quercus section Quercus) represent a prime example of such a species complex: recent diversification and ongoing frequent hybridization result in vague species delineations, characteristic of a syngameon. However, these blurred boundaries do not imply an absence of distinct evolutionary units. In this project, we want to disentangle species relationships among white oaks in Southeastern Europe, a part of the distribution range that has been historically understudied. We combine whole-genome re-sequencing, plastome and leaf morphology data of 1,205 trees from the white oak species complex across pure and mixed populations spanning from Central Europe to Georgia. By integrating phylogenetic and population genetic approaches combined with morphological characterizations, we address the frequent incongruences found between different datasets. We reconstruct chloroplast lineages to gain insights into the migration routes of Southeastern European white oaks, and compare these with evolutionary histories reconstructed from nuclear data. Our analyses reveal a strong geographic signal in population structure. Plastid haplotypes indicate a mixing of genetic diversity originating from both western and eastern lineages in Southeastern Europe. Moreover, shared chloroplast lineages among species suggest recurrent plastome capture through hybridization. Crucially, despite this evidence of extensive hybridization, phylogenetic trees still recover clear species delimitation. Through a first quantification of gene flow and incomplete lineage sorting, we demonstrate that apparent contradictions between phylogenetic, population genetic, and morphological signals represent direct reflections of dynamic evolutionary processes. While species complexes with porous borders naturally complicate classification, the concept of a syngameon perfectly illustrates how integrative approaches can reconcile conflicts and deepen our understanding of the evolutionary forces shaping biodiversity.
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