Genetic and biometric patterns of rangewide divergence of iconic, Neogene relic broadleaved shrub species Staphylea pinnata L.– post-glacial expansion and human impact

Vegetation History and Archaeobotany https://doi.org/10.1007/s00334-024-01026-3 ORIGINAL ARTICLE Genetic and biometric patterns of rangewide divergence of iconic, Neogene relic broadleaved shrub species Staphylea pinnata L.– postglacial expansion and human impact Łukasz Piechnik1 · Bartosz Łabiszak2 · Elżbieta Cieślak1 · Sebastian Szczepański2 · Przemysław Kurek2 Andriy Novikov4 · Leonardo Rosati5 · Ali A. Dönmez6 · Monika Dering7 · Tomasz Wójcik8 · Blanka Wiatrowska9 · Magdalena Żywiec1 · Witold Wachowiak2,3 · Received: 12 July 2024 / Accepted: 1 November 2024 © The Author(s) 2024 Abstract Integrative phylogeographic studies supported by morphometric analysis and genetic data provide significant insights into the postglacial recolonization history and other factors shaping current distributions of plant species, including major forest-forming trees in Europe. However, genomic resources and phylogeographic knowledge of shrub species remain limited. Staphylea pinnata L. (European bladdernut) is a shrub native to thermophilous broadleaf forests and is the only representative of the Staphyleaceae in Central Europe. Given its historical associations with human and religious beliefs dating back to pre-Christian cultures, the current distribution of this iconic, Neogene relic species has been hypothesized to be influenced by human-assisted migration. This study aims to address this hypothesis by uncovering the genetic and morphometric relationships among S. pinnata populations across its wide distribution range in Europe, Caucasus and the Anatolian Peninsula, linking these findings with existing archaeobotanical and ethnobotanical data. We sampled 87 populations (979 individuals), genotyped them with the applications of newly developed genetic markers, and conducted morphological leafs’ measurements to estimate the postglacial expansion and human impact on the current distribution of S. pinnata. Both genetic and morphometric results indicate primarily natural post-glacial recolonization from two Pleistocene glacial refugia in the Apennines and Balkans. Additionally, we identified “suture zones” of increased genetic diversity in middle latitudes, resulting from secondary contact due to postglacial recolonization from different sources. Significant human contributions were observed towards the northernmost edge of the species’ range, including regions such as Eastern France, Lower Silesia in Poland, and Northern Podolia in Ukraine. Keywords European bladdernut · Neogene species · cpDNA · Genetic diversity · Leaf morphology · Population variability · Geographical differentiation · Human impact Communicated by F. Bittmann. Łukasz Piechnik 1 W. Szafer Institute of Botany, Polish Academy of Sciences, Lubicz 46, Kraków 31-512, Poland 2 Department of Plant Ecology and Environmental Protection, Adam Mickiewicz University, Uniwersytetu Poznańskiego 6, Poznań 61-614, Poland 3 Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, Kórnik 62-035, Poland 4 State Museum of Natural History, National Academy of Sciences of Ukraine, Teatralna 18, Lviv 79008, Ukraine 5 Scuola di Scienze Agrarie, Forestali e Ambientali, Università della Basilicata, Via Ateneo Lucano 10, Potenza 85100, Italy 6 Faculty of Science, Department of Biology, Hacettepe University, Beytepe, Ankara, Türkiye 7 Department of Silviculture, Poznań University of Life Sciences, Wojska Polskiego 71A, Poznań 60-625, Poland 8 Department of Nature Protection and Landscape Ecology, University of Rzeszów, Zelwerowicza 4, Rzeszów 35-601, Poland 9 Department of Botany and Forest Habitats, Poznań University of Life Sciences, Wojska Polskiego 71D, Poznań 60-625, Poland 13 Vegetation History and Archaeobotany Introduction Many phylogeographic studies have investigated the consequences of intrinsic, ecological and geographic barriers as natural determinants of gene flow in plant species (e.g., Feder et al. 2012; Leroy et al. 2020). However, the anthropogenic determinants of gene flow remain largely unexplored (Manel and Holderegger 2013), primarily because addressing these issues requires integration of multiple data sources, including genetic, archaeobotanical, and ecological information. Therefore, detailed studies are needed to gain a full understanding of the direct and indirect impacts of human activity on species distribution (Redman 1999; Moskal-del Hoyo et al. 2018; Novák et al. 2021). In cultivated landscapes extensively altered by prolonged and diverse human activity it is often challenging to determine whether a species is native to a given area or if its presence is purely anthropogenic (Lauterjung et al. 2018; Pokorná et al. 2018). For many woody plant species, their natural distribution range remains unclear due to their long history of cultivation (Stanford et al. 2000; George et al. 2015; Da Ronch et al. 2016). Staphylea pinnata L. (European bladdernut), is one of such species. Especially at the northern edge of its distribution range, its natural origin is frequently questionable (Hendrych 1980; Środoń 1992; Parent 2000). Moreover, this iconic species has been widely used by humans in Central Europe from ancient times to the present (Łuczaj 2009; Heiss et al. 2014; Redžić and Ferrier 2014). Staphylea pinnata is a deciduous, medium-sized shrub with pinnate leaves, olive-gray bark and panicle-shaped, overhanging, white inflorescences. The fruits – two- or three-chambered bloated capsules – contain 1–4 spherical, very hard, smooth, light brown seeds. S. pinnata is the only native representative of the family Staphyleaceae in Central Fig. 1 Natural range of Staphylea pinnata (shown in red). The map was created based on chorology data in Gostyńska 1961; Meusel et al. 1978; Piechnik et al. 2021 and unpubl. data by the authors 13 Europe with the closest relative being Asiatic S. bumalda, endemic to forests in China, Japan, and Korea (Harris et al. 2017). Within the genus Staphylea, 11 species are clustered in three main geographical regions: North America, South and East Asia, Europe and the Middle East. In Europe and the Middle East, there are only two species: S. colchica Stev. (Caucasian bladdernut) and S. pinnata L. (Simmons 2007). The modern geographic range of S. pinnata is disjunctive and refers to the distributional pattern reported for Neogene relicts, e.g., Aesculus L. or Zelkova Spach. It consists of two main parts: Europe and Caucasia-Anatolia (Meusel et al. 1978). The first part of the range covers the countries of southern, south-eastern and central Europe from the Apennine to the Balkan Peninsulas in the south. The northern border of the range consists of disconnected clusters in eastern France, Germany, Czechia, Slovakia, southern Poland and western Ukraine. It also occurs in Georgia, Armenia, Azerbaijan and Krasnodar Krai (Russia) as well as in enclaves in Türkiye, where its exact range is poorly investigated (see Fig. 1). S. pinnata, in most of its natural range, is asso (...truncated)