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Orostachys Spinosa (Crassulaceae) Origin and Diversification: East Asia

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Orostachys Spinosa (Crassulaceae) Origin and Diversification: East Asia Plant Systematics and Evolution (2020) 306:84 https://doi.org/10.1007/s00606-020-01713-4 ORIGINAL ARTICLE Orostachys spinosa (Crassulaceae) origin and diversifcation: East Asia or South Siberian Mountains? Chloroplast DNA data Arthur Yu. Nikulin1 · Vyacheslav Yu. Nikulin1 · Andrey A. Gontcharov1 Received: 20 December 2019 / Accepted: 3 September 2020 © Springer-Verlag GmbH Austria, part of Springer Nature 2020 Abstract Limited data are available on genetic structures of the herbaceous plant species populations inhabiting mountainous areas of Siberia and Northeastern Asian (Russian Far East). Although this area was not directly impacted by the extensive ice-sheets during the Quaternary, it experienced signifcant climatic fuctuations that infuenced rich local fora. Orostachys spinosa (Crassulaceae) lacks any adaptations for long-distance dispersal, yet the species is characterized by an unusually wide range spanning from the Urals to the coast of the Pacifc Ocean. We studied O. spinosa phylogeography and genetic diversity across its range sampling 203 individuals from 21 natural populations. Using sequences from three chloroplast DNA non- coding regions, we revealed 82 haplotypes and observed high level of population diferentiation indicating presence of the phylogeographic structure (GST = 0.501 and NST = 0.822 (p < 0.01)). In concordance with the previous phylogenetic analyses based on ITS rDNA data, parsimony network revealed two distinct cpDNA haplotype lineages deferring in their structure and characteristics of genetic diversity. The split between these haplotype groups can be dated to the Pliocene (ca. 3.6 Mya). According to our estimates diversifcation in the Western group of populations took place ca. 1 Mya earlier than in the East- ern group (3.1 Mya and 2.26 Mya, respectively). Apart from the generally accepted notion about East Asian origin of O. spinosa, our results indicated that the species could have originated in mountains of Southern Siberia (Altai). This region was colonized independently from O. thyrsifora which has a largely overlapping distribution in this area. Keywords Altai · cpDNA haplotypes · Genetic structure · Origin · Orostachys spinosa · Phylogeography Introduction 2015; Li et al. 2012; Wroblewska 2012; Chen et al. 2014; Fu et al. 2016; Zhang et al. 2018). The patterns of genetic A number of studies have documented signifcant genetic diversity in these taxa have been shaped by the interaction diversity in plant species associated with the temperate of many factors, such as life history traits, ecological vari- mountainous areas of Europe, Northern America, and East- ables (e.g., life cycle, breeding system, pollination and dis- ern Asia (e.g., Stehlik et al. 2002; Tribsch and Schönswetter persal mechanisms, efective population size, connectivity, 2003; Ronikier et al. 2008; Cun and Wang 2010; Xu et al. etc.; Loveless and Hamrick 1984; Eckert et al. 2008; Palstra 2010; Ansell et al. 2011; Allen et al. 2012; Gussarova et al. and Ruzzante 2008), and historical events. The mountain ranges act as a barrier to species migration (Taberlet et al. 1998), but due to their complex topography and varied Handling Editor: Mike Thiv. habitat types, they also serve as a refuge during climate oscillations (Tribsch and Schönswetter 2003). The efects Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s0060 6-020-01713 -4) contains of the climate changes on plant species’ geographical dis- supplementary material, which is available to authorized users. tributions and population demographies are considerable, involving latitudinal and altitudinal migrations, population * Arthur Yu. Nikulin extinction, and range fragmentation/expansion that leaves [email protected] long-lasting, detectable genetic imprints within and among 1 Federal Scientifc Center of the East Asia Terrestrial species (Abbott et al. 2000; Avise 2000; Hewitt 2000, 2004, Biodiversity of the Far Eastern Branch, Russian Academy 2011; Qiu et al. 2013; Wen et al. 2014, 2016). of Sciences, 100-Letia Vladivostoka Prospect, 159, Vladivostok, Russia 690022 Vol.:(0123456789)1 3 84 Page 2 of 14 A. Yu. Nikulin et al. Still relatively little is known about the genetic structures among species of the genus Hylotelephium H. Ohba (Mayu- of the plant species that are restricted to the mountains and zumi and Ohba 2004; Gontcharova et al. 2006; Nikulin et al. adjacent Siberia and Northeastern Asian (Russian Far East) 2015b). The clade Appendiculatae was resolved as a sister areas which are characterized by rich local foras (Krasnob- to the Hylotelephium/Orostachys lineage and harbored the orov 1976; Malyshev and Peshkova 1984; Revushkin 1988; monotypic genus Meterostachys. These patterns of phylo- Stepanov et al. 2003; Malyshev et al. 2012). Genetic data genetic relationships require a number of taxonomic adjust- are very scarce for herbaceous species having wide distribu- ments (e.g., classifcation of Hylotelephium species under tion areas spanning Circumboreal and Eastern Asiatic phy- the name Orostachys and Orostachys subsection Appen- togeographic zones (Takhtajan 1986). Such contemporary diculatae members under the name Meterostachys; Nikulin distribution patterns could be remnants of an ancient range et al. 2015a, b). The divergence time estimation showed that or a result of the recent range expansion. Although south- O. spinosa diverged from its closest relatives circa 6.5 Mya ern Siberian Mountains were not directly impacted by the (Late Miocene). Analyses of multiple O. spinosa ITS rDNA unifed ice-sheets during the Quaternary, they experienced sequences revealed a split between specimens from west- a much cooler and dryer climate during the glacial periods ern and eastern parts of the species range dated to 3.5 Mya (Sun and Chen 1991) and likely served as refugia for many (Nikulin et al. 2015b). Diversifcation in the Western lineage organisms (Schmitt and Varga 2012). These climatic fuctua- (includes ribotypes found in Siberia and Northeastern Asia) tions should have signifcant efects on the genetic structure also took place in the Late Pliocene circa 3 Mya, while in of the local biota, but the responses of local plants to the the Eastern lineage (ribotypes from the northeast of China glaciation are still poorly understood. High levels of genetic and south of the Russian Far East), it started much later in diversity are expected for areas that are thought to be refu- the Early Pleistocene, circa 1.2 Mya, but still long before the gial (such as Altai, Sayan, Sikhote-Aline Mountains). These last glaciation period. refugia were mostly confned to the mountainous regions Although the O. spinosa concept has never been ques- because they enjoyed relative stability during the Quaternary tioned, it was noted that populations in the eastern part of climatic cycles due to moisture availability (orographic rain- the range are represented by individual monocarpic rosettes, fall), and their diverse topographies have provided sheltered whereas in the more continental western areas, the same spe- habitats from the cold winds (Fjeldsaå and Lovett 1997; cies shows diferent growth habits with numerous densely Tzedakis et al. 2002; Kaltenrieder et al. 2009; Médail and crowded vegetative rosettes (Bezdeleva 1995; Gontcharova Diadema 2009; Muellner-Riehl 2019). Importantly, an altitu- 2006). It remains unclear whether these morphotypes refect dinal retreat of only 10 m might be equivalent to an approxi- distinct genotypes or resulted from adaptations to more xeric mately 10 km latitudinal retreat (Jump et al. 2009); therefore, environments. mountains allow plant species to follow warm interglacial/ This study provides molecular data for a better under- cold glacial trends by means of relatively narrow altitudinal standing of the evolutionary history of the Asian crassu- shifts instead of larger latitudinal migrations. lacean fora, specifcally the relationships between O. spi- Orostachys spinosa (L.) Sweet is one of the species nosa populations. We characterized wide-range patterns of characterized by an unusually wider range than most other genetic diversity in the species focusing on the contrasts in crassulacean taxa. It covers a signifcant part of Northern genetic diferentiation between western and eastern popula- Asia from the coast of the Pacifc Ocean to the Urals. This tions and examining the species’ phylogeography based on species grows on rock crevices and dry slopes at sea level intergenic plastid DNA sequences. up to 3000 m altitude. The seeds lack any specifc adap- tations for long-distance dispersal thus falling close to the maternal plant. They are small and light, produced in high Materials and methods quantities, and can be dispersed a limited distance by wind. The species’ broad altitudinal and latitudinal ranges imply Plant materials substantial thermal tolerance that along with adaptation to xeric conditions, may have enhanced survival during the Leaves or inforescences were sampled from 21 O. spinosa Late Pleistocene. (203 individuals) and one O. japonica (Maxim.) A.Berger Orostachys spinosa is a member of the East Asian cras- (10 individuals) natural populations (Table 1; Fig. 1) cover- sulacean genus Orostachys Fisch., and along with fve more ing most of the distribution range of this species. species, is part of subsection Appendiculatae (Borissova) H. The sample size was from eight to ffteen individuals per Ohba (Eggli 2005). Taxomonic relationships in the genus are population, except for fve populations (P3,
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