Polyploidy and hybridization in the Mediterranean: unravelling the evolutionary history of Centaurium (Gentianaceae)

Ana Valdés-Florido; Claudia González-Toral; Enrique Maguilla; Eduardo Cires; Zoila Díaz-Lifante; Cristina Andrés-Camacho; Gonzalo Nieto Feliner; Juan Arroyo; Marcial Escudero

doi:10.1093/aob/mcae066

Polyploidy and hybridization in the Mediterranean: unravelling the evolutionary history of Centaurium (Gentianaceae)

Ann Bot. 2024 Apr 30:mcae066. doi: 10.1093/aob/mcae066. Online ahead of print.

Authors

Ana Valdés-Florido¹, Claudia González-Toral², Enrique Maguilla³, Eduardo Cires^{2

4}, Zoila Díaz-Lifante¹, Cristina Andrés-Camacho¹, Gonzalo Nieto Feliner⁵, Juan Arroyo¹, Marcial Escudero¹

Affiliations

¹ Department of Plant Biology and Ecology, Faculty of Biology, University of Seville, 41012, Seville, Spain.
² Department of Organisms and Systems Biology, University of Oviedo, 33071, Oviedo, Spain.
³ Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, 41013, Seville, Spain.
⁴ Institute of Natural Resources and Territorial Planning (INDUROT), Campus de Mieres, 33600 Mieres, Spain.
⁵ Real Jardín Botánico (RJB), CSIC, Plaza de Murillo 2, 28014, Madrid, Spain.

PMID: 38687133
DOI: 10.1093/aob/mcae066

Abstract

Background and aims: Polyploidy is considered one of the main mechanisms of plant evolution and speciation. In the Mediterranean basin, polyploidy has contributed to making this region a biodiversity hotspot, along with its geological and climatic history and other ecological and biogeographic factors. The Mediterranean genus Centaurium Hill (Gentianaceae) comprises ca. 25 species, of which 60% are polyploids, including tetraploids and hexaploids. To date, the evolutionary history of centauries has been studied using Sanger sequencing phylogenies, which have been insufficient to fully understand the phylogenetic relationships in this lineage. The goal of this study is to gain a better understanding of the evolutionary history of Centaurium by exploring the mechanisms that have driven its diversification, specifically hybridization and polyploidy. We aim at identifying the parentage of hybrid species, at the species or clade level, as well as assessing whether morphological traits are associated with particular ploidy levels.

Methods: We sequenced RADseq markers from 42 samples of 28 Centaurium taxa, and performed phylogenomic analyses using maximum likelihood, summary coalescent SVDquartets and NeighborNet approaches. To identify hybrid taxa, we used Phylonetworks and the fastStructure algorithm. To infer the putative parental species of the allopolyploids, we employed genomic analyses (SNIPloid). The association between different traits and particular ploidy levels was explored with NMDS.

Key results: Our phylogenetic analyses confirmed the long-suspected occurrence of recurrent hybridization. The allopolyploid origin of the tetraploid C. serpentinicola and the hexaploids C. mairei, C. malzacianum and C. centaurioides were also confirmed, unlike that of C. discolor. We inferred additional signatures of hybridization events within the genus and identified morphological traits differentially distributed in different ploidy levels.

Conclusions: This study highlights the important role that hybridization has played in the evolution of a Mediterranean genus such as Centaurium, leading to a polyploid complex, which facilitated its diversification and may exemplify that of other Mediterranean groups.

Keywords: Mediterranean; RADseq; allopolyploidy; centauries; hybridization; plant evolution; polyploidy.