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UC Berkeley UC Berkeley Previously Published Works UC Berkeley UC Berkeley Previously Published Works Title Widespread co-occurrence of multiple ploidy levels in fragile ferns (Cystopteris fragilis complex; Cystopteridaceae) probably stems from similar ecology of cytotypes, their efficient dispersal and inter-ploidy hybridization. Permalink https://escholarship.org/uc/item/8516c3z8 Journal Annals of botany, 123(5) ISSN 0305-7364 Authors Hanušová, Kristýna Čertner, Martin Urfus, Tomáš et al. Publication Date 2019-05-01 DOI 10.1093/aob/mcy219 Peer reviewed eScholarship.org Powered by the California Digital Library University of California BList1=SubBList1=BList1=SubBList BList1=SubBList3=BList1=SubBList2 Annals of Botany XX: 1–11, 2018 SubBList1=SubSubBList3=SubBList1=SubSubBList2 doi: 10.1093/aob/mcy219, available online at www.academic.oup.com/aob 2018 December 18 on Hall) user (Boalt Law of School California of by University https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcy219/5240163 from Downloaded SubSubBList3=SubBList=SubSubBList=SubBList SubSubBList2=SubBList=SubSubBList=SubBList SubBList2=BList=SubBList=BList Keywords=Keywords=Keywords_First=Keywords Widespread co-occurrence of multiple ploidy levels in fragile ferns (Cystopteris Keywords=HeadA=Keywords_Last=HeadA fragilis complex; Cystopteridaceae) probably stems from similar ecology of HeadA=HeadB=HeadA=HeadB/HeadA cytotypes, their effcient dispersal and inter-ploidy hybridization HeadB=HeadC=HeadB=HeadC/HeadB 1 1,2 1 3 3 4 HeadC=HeadD=HeadC=HeadD/HeadC Kristýna Hanušová , Martin Čertner , Tomáš Urfus , Petr Koutecký , Jiří Košnar , Carl J. Rothfels , Vlasta Jarolímová2, Jan Ptá ek1 and Libor Ekrt3* Extract3=HeadA=Extract1=HeadA č CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA 1Department of Botany, Faculty of Science, Charles University, Benátská 2, CZ-128 00 Praha, Czech Republic, 2Institute of CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB Botany, The Czech Academy of Sciences, Zámek 1, CZ-252 43 Průhonice, Czech Republic, 3Department of Botany, Faculty 4 CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC of Science, University of South Bohemia, Branišovská 1760, CZ-370 05 České Budějovice, Czech Republic, and University Herbarium and Department of Integrative Biology, University of California, Berkeley, CA 94720, USA CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA * For correspondence. E-mail [email protected] ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB Received: 15 July 2018 Returned for revision: 17 September 2018 Editorial decision: 6 November 2018 Accepted: 9 November 2018 ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC • Background and Aims Polyploidy has played an important role in the evolution of ferns. However, the dearth ERR_Extract3=ERR_HeadA=ERR_Extract1=ERR_HeadA of data on cytotype diversity, cytotype distribution patterns and ecology in ferns is striking in comparison with SectionTitle=SectionTitle=SectionTitle=SectionTitle1 angiosperms and prevents an assessment of whether cytotype coexistence and its mechanisms show similar pat- terns in both plant groups. Here, an attempt to fll this gap was made using the ploidy-variable and widely distrib- App_Head=App_HeadA=App_Head=App_HeadA/App_Head uted Cystopteris fragilis complex. HeadB=Text=HeadB=TextInd • Methods Flow cytometry was used to assess DNA ploidy level and monoploid genome size (Cx value) of 5518 C. fragilis individuals from 449 populations collected over most of the species’ global distributional range, supplemented with data from 405 individuals representing other related species from the complex. Ecological preferences of C. fragilis tetraploids and hexaploids were compared using feld-recorded parameters and database- extracted climate data. • Key Results Altogether, fve different ploidy levels (2x, 4x, 5x, 6x, 8x) were detected and three species exhib- ited intraspecifc ploidy-level variation: C. fragilis, C. alpina and C. diaphana. Two predominant C. fragilis cyto- types, tetraploids and hexaploids, co-occur over most of Europe in a diffuse, mosaic-like pattern. Within this contact zone, 40 % of populations were mixed-ploidy and most also contained pentaploid hybrids. Environmental conditions had only a limited effect on the distribution of cytotypes. Differences were found in the Cx value of tetraploids and hexaploids: between-cytotype divergence was higher in uniform-ploidy than in mixed-ploidy populations. • Conclusions High ploidy-level diversity and widespread cytotype coexistence in the C. fragilis complex match the well-documented patterns in some angiosperms. While ploidy coexistence in C. fragilis is not driven by envi- ronmental factors, it could be facilitated by the perennial life-form of the species, its reproductive modes and eff- cient wind dispersal of spores. Independent origins of hexaploids and/or inter-ploidy gene fow may be expected in mixed-ploidy populations according to Cx value comparisons. Keywords: Bladder ferns, contact zone, Cx value, Cystopteris fragilis, cytotype coexistence, ecological prefer- ences, fow cytometry, genome size, ploidy distribution, pteridophytes. INTRODUCTION and genome size are tightly correlated in this plant group, unlike in angiosperms (Barker, 2013; Clark et al., 2016). High Polyploidization (whole-genome duplication) is widely consid- accumulation of polyploidy in some fern lineages (Clark et al., ered one of the major forces contributing to the evolutionary 2016; Schneider et al., 2017) makes them suitable models for diversifcation of land plants (Soltis et al., 2016; Landis et al., studying polyploid evolution. 2018). This is especially so in ferns, where approx. 30 % of The prevailing mode of polyploid origin is via unreduced speciation events are presumably linked to changes in ploidy, gametes (i.e. gametes with a somatic chromosome number), twice the rate predicted for angiosperms (Wood et al., 2009). produced as a consequence of rare meiotic errors (Ramsey, Specifcally, by providing immediate postzygotic reproductive 2007; Kreiner et al., 2017). The rarity of polyploid formation isolation between newly arisen polyploids and their progenitors, is compounded by demographic challenges: new polyploids polyploidization is an effcient mechanism of sympatric spe- generally suffer from a lack of compatible mating partners, ciation (Ramsey and Schemske, 1998; Coyne and Orr, 2004). and crosses with their progenitors, which produce sterile Polyploidization was suggested as the predominant mechanism odd-ploidy offspring, may lead to their extirpation (‘minority of genome size expansion in ferns, and chromosome number cytotype exclusion’; Levin, 1975). The frequency-dependent © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected]. 2 Hanušová et al. — Cytogeography of Cystopteris fragilis complex Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcy219/5240163 by University of California School of Law (Boalt Hall) user on 18 December 2018 December 18 on Hall) user (Boalt Law of School California of by University https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcy219/5240163 from Downloaded selection driving this process may similarly affect otherwise an extremely wide geographical distribution (Rothfels et al., well-established cytotypes if they meet in contact zones, 2013), but whether spatial isolation of cytotypes or their sort- which makes minority cytotype exclusion a main constraint ing along ecological gradients contributes to cytotype coex- to ploidy coexistence in general (Husband, 2000). In recent istence remains unknown. Lastly, our preliminary ploidy decades, several mechanisms facilitating successful polyploid screening in Central Europe revealed a high frequency of establishment and/or cytotype coexistence have been proposed mixed-ploidy populations in C. fragilis. We used a wide array (reviewed by Kolář et al., 2017). For example, the minority of complementary approaches, consisting of extensive feld status of one of the coexisting cytotypes may be overcome by sampling, fow cytometric analysis of ploidy level and relative its recurrent origin (Ramsey, 2007), effcient vegetative spread genome size, and ecological niche comparisons, to investigate (Chrtek et al., 2017), autogamy (Petit et al., 1997), non-ran- the following questions: (1) What is the cytotype diversity in dom mating (Husband et al., 2008) or a substantial competitive the C. fragilis complex and how is it geographically distrib- advantage (Felber, 1991). Prominent among these mechanisms uted (with a focus on Europe and North America)? (2) Could is the (fne-scale) spatial segregation of cytotypes, which can monoploid genome size comparisons provide additional clues increase the rate of compatible, within-ploidy mating (Baack, to the evolution of cytotypes? (3) How common and wide- 2005; Kolář et al., 2017). The most frequently reported cause of spread is cytotype coexistence in C. fragilis? (4) Is cytotype such spatial segregation of cytotypes is their different ecologi- coexistence in C. fragilis driven by the underlying environ- cal preferences (e.g. Levin, 2002; Laport et al., 2016). mental heterogeneity? Cytogeography, the study of cytotype diversity and its dis- tribution patterns, is usually the frst step towards understand- MATERIALS AND METHODS ing the mechanisms of polyploid evolution (Soltis et al., 2003). Cytotype distribution patterns
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