Homoplastic versus xenoplastic evolution: exploring the emergence of key intrinsic and extrinsic traits in the montane genus Soldanella (Primulaceae)

• Published in: The Plant journal : for cell and molecular biology 2024-05, Vol.118 (3), p.753-765
• Main Authors: Rurik, Ivan, Melichárková, Andrea, Gbúrová Štubová, Eliška, Kučera, Jaromír, Kochjarová, Judita, Paun, Ovidiu, Vďačný, Peter, Slovák, Marek
• Format: Article
• Language: English
• Subjects: Biological Evolution; Convergence; convergent evolution; Ecological conditions; European alpine system; Evolution; genome size; Genome, Plant - genetics; Genomes; Hybridization; Hybridization, Genetic; Mountain environments; Phenotype; Phenotypes; phylogenetic networks; phylogenetic regression; Phylogenetics; Phylogeny; Soldanella; Styrax; trait reconstruction
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.16630

SUMMARY Specific ecological conditions in the high mountain environment exert a selective pressure that often leads to convergent trait evolution. Reticulations induced by incomplete lineage sorting and introgression can lead to discordant trait patterns among gene and species trees (hemiplasy/xenoplasy), providing a false illusion that the traits under study are homoplastic. Using phylogenetic species networks, we explored the effect of gene exchange on trait evolution in Soldanella, a genus profoundly influenced by historical introgression. At least three features evolved independently multiple times: the single‐flowered dwarf phenotype, dysploid cytotype, and ecological generalism. The present analyses also indicated that the recurring occurrence of stoloniferous growth might have been prompted by an introgression event between an ancestral lineage and a still extant species, although its emergence via convergent evolution cannot be completely ruled out. Phylogenetic regression suggested that the independent evolution of larger genomes in snowbells is most likely a result of the interplay between hybridization events of dysploid and euploid taxa and hostile environments at the range margins of the genus. The emergence of key intrinsic and extrinsic traits in snowbells has been significantly impacted not only by convergent evolution but also by historical and recent introgression events. Significance Statement The captivating phenomenon of convergent trait evolution in response to particular environmental conditions is a hallmark of biology. Nonetheless, the substantial historical introgression holds the capacity to introduce distinct traits to species influenced by this gene flow, thus misleadingly resembling genuine evolutionary convergence.