Whole-genome analyses disentangle reticulate evolution of primroses in a biodiversity hotspot

Biodiversity hotspots, such as the Caucasus mountains, provide unprecedented opportunities for understanding the evolutionary processes that shape species diversity and richness. Therefore, we investigated the evolution of Primula sect. Primula, a clade with a high degree of endemism in the Caucasus. We performed phylogenetic and network analyses of whole-genome resequencing data from the entire nuclear genome, the entire chloroplast genome, and the entire heterostyly supergene. The different characteristics of the genomic partitions and the resulting phylogenetic incongruences enabled us to disentangle evolutionary histories resulting from tokogenetic vs cladogenetic processes. We provide the first phylogeny inferred from the heterostyly supergene that includes all species of Primula sect. Primula. Our results identified recurrent admixture at deep nodes between lineages in the Caucasus as the cause of non-monophyly in Primula. Biogeographic analyses support the 'out-of-the-Caucasus' hypothesis, emphasizing the importance of this hotspot as a cradle for biodiversity. Our findings provide novel insights into causal processes of phylogenetic discordance, demonstrating that genome-wide analyses from partitions with contrasting genetic characteristics and broad geographic sampling are crucial for disentangling the diversification of species-rich clades in biodiversity hotspots.

Automated summary

This study investigates the evolutionary processes of Primula sect. Primula in the Caucasus mountains, a biodiversity hotspot. By analyzing whole-genome resequencing data, the study identifies the recurrent admixture between lineages as the cause of non-monophyly in Primula sect. Primula. Biogeographic analyses support the 'out-of-the-Caucasus' hypothesis, highlighting the significance of the Caucasus as a cradle for biodiversity. These findings provide insights into the diversification of species-rich clades in biodiversity hotspots.