Phylogenomics of Southern European Taxa in the Ranunculus auricomus Species Complex: The Apple Doesn’t Fall Far from the Tree

Abstract

The taxonomic status of many Southern European taxa of the Ranunculus auricomus complex remains uncertain despite this region’s proximity to the native ranges of the sexual progenitor species of the complex. We investigated whether additional sexual progenitor species are present in the Mediterranean region. Utilizing target enrichment of 736 single-copy nuclear gene regions and flow cytometry, we analyzed phylogenomic relationships, the ploidy level, and the reproductive mode in representatives of 16 populations in Southern Europe, with additional sequence data from herbarium collections. Additionally, phased sequence assemblies from suspected nothotaxa were mapped to previously described sexual progenitor species in order to determine hybrid ancestry. We found the majority of Mediterranean taxa to be tetraploid, with hybrid populations propagating primarily via apomixis. Phylogenomic analysis revealed that except for the progenitor species, the Mediterranean taxa are often polyphyletic. Most apomictic taxa showed evidence of mixed heritage from progenitor species, with certain progenitor genotypes having mapped more to the populations from adjacent geographical regions. Geographical trends were found in phylogenetic distance, roughly following an east-to-west longitudinal demarcation of the complex, with apomicts extending to the southern margins. Additionally, we observed post-hybridization divergence between the western and eastern populations of nothotaxa in Southern Europe. Our results support a classification of apomictic populations as nothotaxa, as previously suggested for Central Europe.

Navigating phylogenetic conflict and evolutionary inference in plants with target capture data

“…This is commonly achieved in target-capture data through HybPhaser (Nauheimer et al 2021), and has been shown to be highly effective in cases of neoallopolyploidy (e.g. Bloesch et al 2022;Bradican et al 2023); however the method requires careful selection of the presence of diploid references for putative parental clades, and is often unsuitable for groups with complex or ancient reticulation (e.g. McLay et al 2023).…”

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“…Furthermore, we incorporate studies of groups of dwarfed and robust forms from boreal Fennoscandia subjected to artificial cold and temperate climate regimes, recording the morphological traits in order to examine the phenotypic plasticity in response to climate. As previous studies would seem to indicate that sexual reproduction is rare in populations present at the margins of this group's range, we examine whether this extends to Northern Europe where the populations are typically less isolated and more numerous than those in Southern Europe (Ericsson, 2001;Bradican et al, 2023). Although phenotype has previously been the basis for the classification of many of the taxa in this species complex, more recent research has demonstrated in multiple cases that the morphological taxa are often polyphyletic when sequence data are taken into consideration (George et al, 2014;Bradican et al, 2023;Hodacě t al., 2023).…”

“…As previous studies would seem to indicate that sexual reproduction is rare in populations present at the margins of this group's range, we examine whether this extends to Northern Europe where the populations are typically less isolated and more numerous than those in Southern Europe (Ericsson, 2001;Bradican et al, 2023). Although phenotype has previously been the basis for the classification of many of the taxa in this species complex, more recent research has demonstrated in multiple cases that the morphological taxa are often polyphyletic when sequence data are taken into consideration (George et al, 2014;Bradican et al, 2023;Hodacě t al., 2023). To date, it is unclear whether the relatively widespread R. monophyllus morphogroup represents a distinct lineage, as opposed to the many mosaic-like hybrid networks typical of this group (Karbstein et al, 2022).…”

“…Hybrid genotypes are typically polyploid, most often tetraploid or hexaploid, and propagate via apomixis to varying degrees (Nogler, 1984;Hörandl, 1998;Barke et al, 2020). Some populations, for example in Southern Europe, seem to be obligate apomicts (Bradican et al, 2023). Morphological diversity in the group is found in the variety of plant heights, basal and stem leaf shapes, petal sizes, and number of stems and basal leaves, among other traits (Marklund, 1961a;Marklund, 1961b;Ericsson, 2001).…”

“…To date, it is unclear whether the relatively widespread R. monophyllus morphogroup represents a distinct lineage, as opposed to the many mosaic-like hybrid networks typical of this group (Karbstein et al, 2022). In the case of hybrid populations, certain geographic trends in the admixture involving several sexual progenitor species have been observed in Europe, proceeding along longitudinal gradients (Karbstein et al, 2022;Bradican et al, 2023).…”