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

Abstract

Summary 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.

The genomes of Darwin's primroses reveal chromosome‐scale adaptive introgression and differential permeability of species boundaries

“…The phenomenon of a three‐species hybrid has been recorded in other Primula studies (Taylor & Woodell, 2008), so it is possible that this was once a tri‐species hybrid zone. Previous work has proposed chloroplast capture as a cause of cytonuclear discordance in Primula , particularly with regard to the contrasting phylogenetic position of different populations of P. vulgaris and P. elatior between the nuclear and chloroplast phylogenies (Stubbs et al ., 2023). Here, we have provided evidence of unilateral introgression of the chloroplast across species boundaries driving the cytonuclear discordance in this section.…”

“…Reading mapping and variant calling followed Stubbs et al . (2023), and details can be found in Methods S2.…”

“…Samples were sequenced on the Illumina NovaSeq 6000 S4 (paired-end 150-bp reads) to an average depth of 209. Reading mapping and variant calling followed Stubbs et al (2023), and details can be found in Methods S2. Fig.…”

“…Pure individuals are indicated with primary colors, that is P. elatior (blue), P. veris (yellow), P. vulgaris (red), hybrids are indicated with secondary colors, that is P. elatior 9 P. veris hybrids (green), P. veris 9 P. vulgaris hybrids (orange), and P. elatior 9 P. vulgaris hybrids (purple). (a) Schematic phylogeny (based on Stubbs et al, 2023) showing relationships between the three species (solid lines) and described previously degrees of interspecific crossability (dashed lines). Thicker lines between species pairs represent higher crossability.…”

“…inconsistencies between nuclear and cytoplasmic phylogenies) and can occur in the absence of nuclear introgression between the hybridizing species (Rieseberg & Soltis, 1991; Tsitrone et al ., 2003). Chloroplast capture has been documented in several plant systems and is proposed to have occurred in Primula (Guggisberg et al ., 2009; Stubbs et al ., 2023), yet has never been documented on a genomic scale.…”