Evolution of hygrophytic plant species in the Anatolia–Caucasus region: insights from phylogenomic analyses ofCardamineperennials

Abstract

Background and Aims Southwestern Asia is a significant centre of biodiversity and a cradle of diversification for many plant groups, especially xerophytic elements. In contrast, little is known about the evolution and diversification of hygrophytic flora. To fill this gap, we focus on Cardamine (Brassicaceae) species that grow in wetlands over a wide altitudinal range. We aimed to elucidate their evolution, assess the extent of presumed historical gene flow between species, and draw inferences about intraspecific structure. Methods We applied the phylogenomic Hyb-Seq approach, ecological niche analyses, and multivariate morphometrics to a total of 85 Cardamine populations from the target region of Anatolia-Caucasus, usually treated as four to six species, and supplemented them with close relatives from Europe. Key Results Five diploids are recognised in the focus area, three of which occur in regions adjacent to the Black and/or Caspian Seas (C. penzesii, C. tenera, C. lazica), one species widely distributed from the Caucasus to Lebanon and Iran (C. uliginosa), and one western Anatolian entity (provisionally as C. cf. uliginosa). Phylogenomic data suggest recent speciation during the Pleistocene, likely driven by both geographical separation (allopatry) and ecological divergence. With the exception of a single hybrid (allotetraploid) speciation event proven for C. wiedemanniana, an endemic of southern Turkey, no significant traces of past or present interspecific gene flow were observed. Genetic variation within the studied species is spatially structured, suggesting reduced gene flow due to geographical and ecological barriers, but also glacial survival in different refugia. Conclusions This study highlights the importance of the refugial regions of the Black and Caspian Seas for both harbouring and generating hygrophytic species diversity in SW Asia. It also supports the significance of evolutionary links between Anatolia and the Balkan Peninsula. Reticulation and polyploidisation played a minor evolutionary role here in contrast to the European relatives.

Balkan‐Anatolian biogeographic links and the evolutionary significance of Anatolian mountains, as evidenced by Cardamine (Brassicaceae)

“…This is the most widespread, genetically and morphologically complex species among the Cardamine hygrophytes in Southwestern Asia. The centres of its distribution and genetic diversity are in northern Anatolia and the Caucasus (Kantor & al., 2023 and present results), which provide favourable ecological conditions with numerous peaks reaching into the (sub)alpine zone and high humidity from the adjacent Black and Caspian Seas even during climatic oscillations (Parolly, 2020). We found that its genetic variation in northeastern Anatolia is highly structured geographically, with four adjacent but allopatric clades (Anat A–Anat D) revealed from the targeted nuclear genes.…”

“…Divergence time estimates suggested that this lineage originated in the late Pliocene (Kantor & al., 2023), and we assume that it had a broader range encompassing both the Balkans and western Anatolia. The restricted gene flow between populations in the Balkans and western Anatolia, caused by the barriers of the intervening seas and the Thracian lowland area, probably led to genetic differentiation and allopatric speciation, dated to the early Pleistocene (Kantor & al., 2023). Although only a few samples of C. acris were included in the present study, the sister species relationship between C. anatolica and C. acris in both nuclear and plastome data argues for vicariance rather than long-distance dispersal; indeed, the vicariance scenario is supported by our ongoing RADseq study with thorough sampling of C. acris ( Šlenker & al., unpub.).…”

“…Cardamine tenera or C. uliginosa and recorded from Uludağ, was first noted by Šlenker & al. (2021) and then examined by Kantor & al. (2023) in a broader context of related species from Southwestern Asia.…”

“…As a result, biogeographic and evolutionary links between Anatolia and the Balkans have been repeatedly observed (e.g., Ansell & al., 2011; Bilgin, 2011; Kaya & Çıplak, 2017; Falch & al., 2019; Özüdoğru & Mummenhoff, 2020; Carnicero & al., 2021), which are also evidenced here by the phylogenetic lineage of Cardamine acris and C. anatolica . Divergence time estimates suggested that this lineage originated in the late Pliocene (Kantor & al., 2023), and we assume that it had a broader range encompassing both the Balkans and western Anatolia. The restricted gene flow between populations in the Balkans and western Anatolia, caused by the barriers of the intervening seas and the Thracian lowland area, probably led to genetic differentiation and allopatric speciation, dated to the early Pleistocene (Kantor & al., 2023).…”

“…In our recent phylogenomic study focused on two sister lineages of hygrophytic Cardamine (Brassicaceae) species in southwestern Asia, we discovered a divergent position of the population from Uludağ, previously classified as either C. uliginosa or C. tenera (Kantor & al., 2023, see also Cullen, 1965). We proved that C. tenera is a lowland to montane species with a disjunct distribution restricted to the southern Caspian and northeastern Black Sea coast regions, but does not occur in Türkiye.…”