Phylogenomics unravels Quaternary vicariance and allopatric speciation patterns in temperate‐montane plant species: A case study on the Ranunculus auricomus species complex

Abstract

The time frame and geographical patterns of diversification processes in European temperate‐montane herbs are still not well understood. We used the sexual species of the Ranunculus auricomus complex as a model system to understand how vicariance versus dispersal processes in the context of Pleistocene climatic fluctuations have triggered speciation in temperate‐montane plant species. We used target enrichment sequence data from about 600 nuclear genes and coalescent‐based species tree inference methods to resolve phylogenetic relationships among the sexual taxa of the complex. We estimated absolute divergence times and, using ancestral range reconstruction, we tested if speciation was enhanced by vicariance or by dispersal processes. Phylogenetic relationships among taxa were fully resolved with some incongruence in the position of the tetraploid R. marsicus. Speciation events took place in a very short time at the end of the Mid‐Pleistocene Transition (830–580 thousand years ago [ka]). A second wave of intraspecific geographical differentiation occurred at the end of the Riss glaciation or during the Eemian interglacial between 200 and 100 ka. Ancestral range reconstruction suggests a widespread European ancestor of the R. auricomus complex. Vicariance has triggered allopatric speciation in temperate‐montane plant species during the climatic deterioration that occurred during the last phase of the Mid‐Pleistocene Transition. Vegetation restructuring from forest into tundra could have confined these forest species into isolated glacial macro‐ and microrefugia. During subsequent warming periods, range expansions of these species could have been hampered by apomictic derivatives and by other congeneric competitors in the same habitat.

Phylogenomics supported by geometric morphometrics reveals delimitation of sexual species within the polyploid apomictic Ranunculus auricomus complex (Ranunculaceae)

“…We checked the quality of raw reads using FastQC v.0.11.8 (Andrews, 2010). For target enrichment, we selected almost the same samples as in RADseq analyses (see Table 1; Tomasello & al., 2020). Probe design for target enrichment was done from RNA sequences of R. carpaticola, R. cassubicifolius, and R. notabilis published by Pellino & al.…”

“…The application of phylogenomic methods provides a magnitude more loci compared to traditional genetic markers and can resolve relationships of taxa with less than a few million (or even less than 100,000) years of divergence (Pellino & al., 2013;Tripp & al., 2017;Tomasello & al., 2020). Currently, two main approaches are used in species-level systematics: Target enrichment and restriction site-associated DNA sequencing (RADseq; and the similar genotyping-by-sequencing [GBS] method).…”

“…300,000 years ago (Hörandl, 2004). Recently published biogeographical analyses based on single-copy nuclear genes by Tomasello & al. (2020) revealed that vicariance has triggered allopatric speciation of a widespread European, probably forest understory, ancestor and that main speciation events took place ca.…”

So Closely Related and Yet So Different: Strong Contrasts Between the Evolutionary Histories of Species of the Cardamine pratensis Polyploid Complex in Central Europe

“…Microsatellites are efficient, high-resolution genetic markers for both population-and species-level studies (Hodel et al, 2016;Li et al, 2017), and have also been used with success when addressing hybridization events and polyploid evolution (e.g., Sampson and Byrne, 2012;Zozomová-Lihová et al, 2014aFeulner et al, 2019;Hu et al, 2019). The Hyb-Seq approach, which captures target exons with flanking intronic and intergenic regions (Weitemier et al, 2014), allows to resolve relationships at various evolutionary levels from the population level up (Villaverde et al, 2018;Tomasello et al, 2020), including polyploids (e.g., Carter et al, 2019). Our specific aims were to (1) resolve the cytotypic and genetic structure of the species under study, (2) identify intraspecific genetic lineages, potentially reflecting descendants from distinct glacial refugia and postglacial colonization routes, (3) explore if and to what extent the lineages correlate with the cytotypic variation and display different environmental niches, (4) resolve single or polytopic polyploid origins, (5) explore the patterns and extent of hybridization between species and lineages, and, finally, (6) to determine how the structure resolved corresponds with previous taxonomic treatments.…”

The relation of meiotic behaviour to hybridity, polyploidy and apomixis in the Ranunculus auricomus complex (Ranunculaceae)

“…The sexual species, R. notabilis , R. carpaticola, and R. cassubicifolius, are obligate outcrossers [ 32 , 34 ] and can be regarded as progenitors of the whole polyploid complex [ 28 , 35 , 36 ]. R. notabilis and the more closely related species pair R. cassubicifolius/ carpaticola represent two genetically and morphologically distinct lineages that separated c. 600,000 years ago [ 29 , 35 , 37 – 39 ]; all three taxa occur in geographical isolation [map in [ 39 ]]. Functional apomixis in Ranunculus demands effective coupling of apomeiosis and parthenogenetic egg cell generation [ 21 ].…”