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Origin and Genetic Differentiation of Pink-Flowered Sorbus Hybrids in the Western Carpathians

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Origin and Genetic Differentiation of Pink-Flowered Sorbus Hybrids in the Western Carpathians Annals of Botany 120: 271–284, 2017 doi:10.1093/aob/mcx013, available online at https://academic.oup.com/aob PART OF A SPECIAL ISSUE ON POLYPLOIDY IN ECOLOGY AND EVOLUTION Origin and genetic differentiation of pink-flowered Sorbus hybrids in the Western Carpathians Veronika Uhrinova1, Judita Zozomova-Lihov a2, Dana Bernatov a3, Juraj Paule4, Ladislav Paule1 and Dusan Go¨mo¨ry1,* 1Technical University in Zvolen, Faculty of Forestry, TG Masaryka 24, 96053 Zvolen, Slovakia, 2Slovak Academy of Sciences, 3 Institute of Botany, Plant Science and Biodiversity Centre, Dubravsk a cesta 9, 84523 Bratislava, Slovakia, Comenius Downloaded from https://academic.oup.com/aob/article/120/2/271/3069153 by guest on 27 September 2021 University, Botanical Garden, Detached Unit, 03815 Blatnica 315, Slovakia and 4Senckenberg Research Institute and Natural History Museum, Department of Botany and Molecular Evolution, Senckenberganlage 25, 60325 Frankfurt am Main, Germany *For correspondence. E-mail [email protected] Received: 8 November 2016 Returned for revision: 20 December 2016 Editorial decision: 9 January 2017 Accepted: 9 January 2017 Published electronically: 13 March 2017 Background and Aims Diversity of the genus Sorbus has been affected by interspecific hybridizations. Pink- flowered hybrid species have been insufficiently studied so far. They comprise bigenomic hybrid species derived from crosses S. aria s.l. Â S. chamaemespilus and trigenomic ones, where S. aucuparia was involved as well. The main objective of the present study was to reconstruct their hybrid origins as well as to assess genetic distinction among several morphologically recognized hybrid species. Methods Samples from putative maternal species and eight pink-flowered and two white-flowered hybrid species were collected in the Western Carpathians and the Sudetes. In total, 370 specimens were analysed. Six chloroplast microsatellites were used to infer parentage, whereas nuclear amplified fragment length polymorphism (AFLP) markers were employed for the identification of clones and patterns of genetic variation. Ploidy levels were esti- mated by flow cytometry on a subset of 140 individuals. Key Results Genetic data supported their hybrid origins proposed based on flower and leaf morphology, and chlo- roplast DNA (cpDNA) revealed recurrent origins (S. caeruleomontana, S. haljamovae), even from bidirectional hy- bridization events (S. zuzanae). All bigenomic and trigenomic hybrid species (except triploid S. zuzanae)were found to be tetraploid. In addition to polyploidy, low genetic variation and the presence of clones within and among populations were observed, suggesting predominantly apomictic reproduction of the hybrid species. Most of the de- scribed hybrid species appeared also genetically distinct. Conclusions The data suggest that multiple hybridization events in the Western Carpathian Sorbus have led to the formation of separate, partially reproductively isolated genetic lineages, which may or may not be discriminated morphologically. Even bidirectional hybridization can produce individuals classified to the same taxon based on phenotype. For some hybrid taxa, hybridization pathways were proposed based on their genetic proximity to paren- tal species and differences in genome sizes. Key words: Hybridization, allopolyploidy, apomixis, Sorbus chamaemespilus, Sorbus aucuparia, Sorbus aria agg., trigenomic hybrid. in polyploids and highly heterozygous taxa (Savidan, 2000). INTRODUCTION The capacity for apomixis may substantially trigger speciation Hybridization is considered to be an important mechanism of (Jankun, 1993; Whitton et al.,2008). evolution of new species and a bridge for gene flow among spe- Change of ploidy and ongoing hybridization are considered cies (Arnold, 2006). When associated with chromosome dou- major drivers of diversification also in the genus Sorbus and bling (allopolyploidy), it frequently leads to changes in were studied by many authors using morphological, biochemi- morphology and physiology of hybrid offspring and reproduc- cal and genetic approaches (Liljefors, 1955; Warburg and tive isolation from the parents; such newly formed genetic line- Karpati, 1968; Challice and Kovanda, 1978; Aldasoro et al., ages may eventually be recognized as new hybrid species. 1998; Nelson-Jones et al., 2002; Robertson et al.,2004, 2010; According to Mallet (2005) at least 25 % of plant species and Chester et al., 2007; Feulner et al., 2014). In Europe, this genus 10 % of animal species are involved in hybridization. Soltis and comprises five mostly diploid and sexual species (S. aucuparia, Soltis (2009) even suggested that ‘perhaps all angiosperms S. chamaemespilus, S. aria, S. domestica, S. torminalis). All of have likely undergone at least one round of polyploidization them except S. domestica participate in interspecific hybridiza- and hybridization has been an important force in generating an- tions, giving rise to numerous hybrid species. These hybrid taxa giosperm species diversity’. Additionally, hybridization is also can be divided into two major groups: (1) white-flowered presumed to be crucial to the evolution of apomixis (asexual re- nothosubgenera Soraria and Tormaria (Majovskyand production through seeds), which is found almost exclusively Bernatova, 2001) and (2) pink-flowered nothosubgenera VC The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 272 Uhrinova et al. — Origin and genetic differentiation of pink-flowered Sorbus hybrids Chamaespilaria and Chamsoraria (Majovsky and Bernatova, length polymorphisms) and maternally inherited (plastid micro- 2001). Trigenomic hybrid species, which combine genomes of satellites) molecular markers, (2) to propose plausible scenarios three parental species, are rarely reported. An example is S. of their formation, and (3) to assess their distinction and differ- intermedia, reported from southern Sweden and Denmark and entiation, bearing in mind that multiple hybrid species were de- naturalized in the British Isles, for which S. aria s.l., S. aucupa- scribed from a single progenitor pair. ria and S. torminalis were identified as parental species (Nelson-Jones et al., 2002). White-flowered hybrid species from the nothosubgenera MATERIALS AND METHODS Soraria and Tormaria have been well studied. Polyploidy, mul- tiple independent origins and facultative pseudogamous apo- Plant material mixis (i.e. asexuality requiring pollination to initiate seed Sampling for DNA analysis was carried out during the flowering formation) were recorded in these groups (e.g. Nelson-Jones seasons 2009 and 2010 and the specimens were determined Downloaded from https://academic.oup.com/aob/article/120/2/271/3069153 by guest on 27 September 2021 et al.,2002; Robertson et al.,2004, 2010; Chester et al.,2007; based on diagnostic morphological characters (Bernatovaand Lepsı et al., 2008; Hajrudinovic et al.,2015). Diploid sexual Majovsky, 2003) either directly in the field or subsequently on hybrids are also reported (Meyer et al., 2014). The maternal the herbarium specimens. For hybrids we follow the classifica- species of these hybrids are usually S. aucuparia (for Soraria) tion of BernatovaandMajovsky (2003), as it offers names for and S. torminalis (for Tormaria), whereas the paternal one is S. most groups of the hybrid species and these names clearly imply aria s.l. (Nelson-Jones et al.,2002; Chester et al., 2007). The the origin of the hybrid subgenera. Leaf samples were collected opposite direction of hybridization occurred as well, but much from putative parental species (S. aria, S. aucuparia, S. chamae- less frequently (Oddou-Muratorio et al., 2001a; Nelson-Jones mespilus) and seven pink-flowered hybrid species (both bige- et al., 2002). There is a variety of pathways of formation of nomic and trigenomic ones) from six locations in the Western polyploid plants (Ramsey and Schemske, 1998). For white- Carpathians, Slovakia (Fig. 2; Supplementary Data Table S1) flowered Sorbus allopolyploids, both formation of tetraploids covering the full previously described morphological variability. through a triploid bridge (Nelson-Jones et al.,2002; Robertson The eighth species, S. diversicolor Bernatova&Majovsky, is et al., 2004) and formation of triploids via hybridization of tet- very rare and we had only one sample available, which was not raploid and diploid parents (Robertson et al., 2004; Pellicer sufficient for the present study. In the case of S. salatini, the indi- et al.,2012) were reported. Additionally, in all Sorbus hybrids viduals were not recovered in the field and herbarium specimens apomixis facilitates the preservation of newly formed genetic were analysed. Two populations of S. sudetica from the lineages and allows them to evolve into separate taxa, even in Krkonose (Giant Mountains) in the Czech Republic (locus classi- cases when sexuality becomes partially or completely restored cus) were also included in the analyses. Our focus was on pink- during their evolution (Jankun, 1993; Ludwig et al.,2013). flowered hybrids, suggesting S. chamaemespilus as one of the Much less attention has been paid to the pink-flowered progenitors. White-flowered Soraria hybrid species growing at Sorbus hybrid species, which are usually shrubs occurring in locations close to the occurrences of S. chamaemespilus in cen- the dwarf-pine vegetation zone at altitudes of 1000–1500 m. In tral Slovakia were included as well, as
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