Phylogenomic inference and demographic model selection suggest peripatric separation of the cryptic steppe ant species Plagiolepis pyrenaica stat. rev.

The ant Plagiolepis taurica Santschi, 1920 (Hymenoptera, Formicidae) is a typical species of the Eurasian steppes, a large grassland dominated biome that stretches continuously from Central Asia to Eastern Europe and is represented by disjunct outposts also in Central and Western Europe. The extent of this biome has been influenced by the Pleistocene climate, and steppes expanded recurrently during cold stages and contracted in warm stages. Consequently, stenotopic steppe species such as P. taurica repeatedly went through periods of demographic expansion and severe isolation. Here, we explore the impact of these dynamics on the genetic diversification within P. taurica. Delimitation of P. taurica from other Plagiolepis species has been unclear since its initial description, which raised questions on both its classification and its spatiotemporal diversification early on. We re-evaluate species limits and explore underlying mechanisms driving speciation by using an integrative approach based on genomic and morphometric data. We found large intraspecific divergence within P. taurica and resolved geographically coherent western and eastern genetic groups, which likewise differed morphologically. A morphometric survey of type material showed that Plagiolepis from the western group were more similar to P. barbara pyrenaica Emery, 1921 than to P. taurica; we thus lift the former from synonymy and establish it as separate species, P. pyrenaica stat. rev. Explicit evolutionary model testing based on genomic data supported a peripatric speciation for the species pair, probably as a consequence of steppe contraction and isolation during the mid-Pleistocene. We speculate that this scenario could be exemplary for many stenotopic steppe species, given the emphasized dynamics of Eurasian steppes.

Homoploid hybrids are common but evolutionary dead ends, whereas polyploidy is not linked to hybridization in a group of Pyrenean saxifrages.

Hybridization and polyploidy are major forces in plant evolution. Homoploid hybridization can generate new species via hybrid speciation, or modify extant evolutionary lineages through introgression. Polyploidy enables instantaneous reproductive isolation from the parental lineage(s) and is often coupled with evolutionary innovations, especially when linked to hybridization. While allopolyploidy is a well-known and common mechanism of plant speciation, the evolutionary role of autopolyploidy might have been underestimated. Here, we studied the saxifrages of Saxifraga subsection Saxifraga in the Pyrenees, which easily hybridise and include polyploid populations of uncertain origin, as a model to unravel evolutionary consequences and origin of hybridization and polyploidy. Additionally, we investigate the phylogenetic relationship between the two subspecies of the endemic S. pubescens to ascertain whether they should rather be treated as different species. For these purposes, we combined ploidy-informed restriction associated DNA analyses, plastid DNA sequences and morphological data on a comprehensive population sample of seven species. Our results unravel multiple homoploid hybridization events at the diploid level between different species pairs, but with limited evolutionary impact. The ploidy-informed analyses reveal that all tetraploid populations detected in the present study belong to the widespread alpine species S. moschata. Although of autopolyploid origin, they are to some extent morphologically differentiated and underwent a different evolutionary pathway than their diploid parent. However, the high plastid DNA diversity and the internal structure within eastern and western population groups suggest multiple origins of the polyploids. Finally, our phylogenetic analyses show that S. pubescens and S. iratiana are clearly not sister lineages, and should consequently be considered as independent species.