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Libor Ekrt 2,5 , Renata Holubov Á 3 , Pavel Tr Á Vn Í Ček 3,4 , and Jan Suda

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Libor Ekrt 2,5 , Renata Holubov Á 3 , Pavel Tr Á Vn Í Ček 3,4 , and Jan Suda American Journal of Botany 97(7): 1208–1219. 2010. S PECIES BOUNDARIES AND FREQUENCY OF HYBRIDIZATION IN THE D RYOPTERIS CARTHUSIANA (DRYOPTERIDACEAE) COMPLEX: 1 A TAXONOMIC PUZZLE RESOLVED USING GENOME SIZE DATA Libor Ekrt 2,5 , Renata Holubov á 3 , Pavel Tr á vn í ý ek 3,4 , and Jan Suda 3,4 2 Department of Botany, Faculty of Science, University of South Bohemia, Brani š ovsk á 31, CZ-370 05 ý esk é Bud ě jovice, Czech Republic; 3 Department of Botany, Faculty of Science, Charles University in Prague, Ben á tsk á 2, CZ-128 01 Prague, Czech Republic; and 4 Institute of Botany, Academy of Sciences of the Czech Republic, Pr ů honice 1, CZ-252 43 Pr ů honice, Czech Republic • Premise of the study : Genome duplication and interspecifi c hybridization are important evolutionary processes that signifi - cantly infl uence phenotypic variation, ecological behavior, and reproductive biology of land plants. These processes played a major role in the evolution of the Dryopteris carthusiana complex. This taxonomically intricate group composed of one diploid ( D. expansa ) and two allotetraploid ( D. carthusiana a n d D. dilatata ) species in Central Europe. Overall phenotypic similarity, great plasticity, and the incidence of interspecifi c hybrids have led to a continuous dispute concerning species circumscription and delimitation. • Methods : We used fl ow cytometry and multivariate morphometrics to assess the level of phenotypic variation and the fre- quency of hybridization in a representative set covering all recognized species and hybrids. • Key results : Flow cytometric measurements revealed unique genome sizes in all species and hybrids, allowing their easy and reliable identifi cation for subsequent morphometric analyses. Different species often formed mixed populations, providing the opportunity for interspecifi c hybridization. Different frequencies of particular hybrid combinations depended primarily on evolutionary relationships, reproductive biology, and co-occurrence of progenitors. • Conclusions : Our study shows that genome size is a powerful marker for taxonomic decisions about the D. carthusiana com- plex and that genome size data may help to resolve taxonomic complexities in this important component of the temperate fern fl ora. Key words : Central Europe; Dryopteris carthusiana ; ferns; fl ow cytometry; interspecifi c hybridization; mixed populations; multivariate morphometrics; nuclear DNA content; polyploidy; Pteridophyta; taxonomy. Hybridization has long been recognized as a prominent force varies by taxon and location ( Ellstrand et al., 1996 ). From a in plant speciation, with up to 70% of extant plants being taxonomic point, species prone to interspecifi c hybridization descendants of interspecifi c hybrids ( Whitham et al., 1991 ). often pose serious problems because gene fl ow may blur spe- Hybridization can have several important evolutionary cies boundaries and affect levels of variability in natural popu- consequences, including increased genetic diversity, the origin lations. Considering the ploidy level of putative parents, of new ecotypes and taxa, and the reinforcement or breakdown homoploid and heteroploid hybridization can be distinguished of reproductive barriers ( Rieseberg, 1997 ). However, interspe- ( Grant, 1971 ; Rieseberg, 1997 ). While heteroploid hybridiza- cifi c crossing may not always be a source of genetic and func- tion is usually quite easy to detect because of the intermediate tional novelty, because resulting hybrids can suffer from number of chromosomes (e.g., using conventional karyological reduced fi tness and thus merely represent evolutionary dead techniques), recognition of homoploid crosses is a more chal- ends ( Seehausen, 2004 ). Similarly, the detrimental effect of hy- lenging task ( Rieseberg and Carney, 1998 ; Kron et al., 2007 ). bridization on the genetic integrity of rare species has been re- Nevertheless, the last decade has seen signifi cant advances in peatedly documented ( Ellstrand, 1992 ; Levin et al., 1996 ). In the understanding of patterns and dynamics of hybrid specia- general, interspecifi c hybridization plays a central role in the tion, catalyzed mainly by the advent of novel molecular ap- evolutionary history of many plant species, although its impact proaches ( Hegarty and Hiscock, 2005 ; Uyeda and Kephart, 2006 ). One of the taxonomically intricate plant groups that have 1 Manuscript received 11 July 2009; revision accepted 17 May 2010. been signifi cantly affected by interspecifi c hybridization (often The authors thank S. Jessen for several plant samples (including D. coupled with genome duplication) is the woodfern ( Dryopteris u sarvelae ) and V. Jarol í mov á for karyological analyses of D. expansa . The Adans., Dryopteridaceae, Pteridophyta) ( Manton, 1950 ). In authors are also grateful to K. Kub á t, E. Ekrtov á , A. H á jek, M. Lep š í , and temperate regions, Dryopteris belongs among the most hybrid- J. Ku þ era for help during fi eldwork and to J. Rauchov á for assistance with prone genera, with almost every combination of species pairs FCM analyses. This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic (project no. MSM 0021620828) and recorded ( Wagner, 1971 ; Fraser-Jenkins, 1982 ; Dost á l et al., the Academy of Sciences of the Czech Republic (no. AV0Z60050516). 1984 ; Frey et al., 1995 ; Krause, 1998 ) as well as one interge- 5 Author for correspondence (e-mail: [email protected]) neric hybrid ( Wagner et al., 1992 ). A paradigmatic example in the Central European fl ora is the Dryopteris carthusiana (for- doi:10.3732/ajb.0900206 merly D. spinulosa ) complex. This conspicuous component of American Journal of Botany 97(7): 1208–1219, 2010; http://www.amjbot.org/ © 2010 Botanical Society of America 1208 July 2010] Ekrt et al. — Taxonomy of DRYOPTERIS CARTHUSIANA complex 1209 temperate woodlands consists of one diploid (2 n = 2 x = 82) spe- heteroploid hybridization ( Manton, 1950 ), while studies of cies D. expansa (C. Presl) Fraser-Jenk. et Jermy and two tetra- chromosome pairing during meiosis in both natural and artifi - ploids (2 n = 4x = 164), D. carthusiana (Vill.) H. P. Fuchs and cial hybrids shed some light on species relationships ( Manton D. dilatata (Hoffm.) A. Gray. The latter (allo)tetraploid has and Walker, 1953 ; Walker, 1955 , 1961 ). In recent years, an- been hypothesized to be derived from a cross between D. ex- other cytogenetic character, genome size, has become accessi- pansa var. alpina (Moore) Viane and D. intermedia subsp. ma- ble ( Leitch and Bennett, 2007 ). The knowledge that genome derensis (Alston) Fraser-Jenk. ( Gibby and Walker, 1977 ; Viane, size is usually constant within the same taxonomic entity 1986 ; Krause, 1998 ), while D. carthusiana is thought to com- ( Greilhuber, 2005 ) but may vary tremendously even among bine genomes of D. intermedia (Muhlenberg ex Willdenow) A. closely related taxa ( Bennett and Leitch, 2005 ) provides a foun- Gray subsp. intermedia from North America and an undiscov- dation for employing genome size as an important taxonomic ered diploid that has been variously identifi ed as D. “ semicris- marker. Indeed, this character has proven successful in resolv- tata ” ( Wagner, 1971 ; Werth and Lellinger, 1992 ) or D. ing complex low-level taxonomies, delimiting species boundar- “ stanley-walkeri ” ( Fraser-Jenkins, 2001 ). The unknown diploid ies, and revealing cryptic taxa ( Dimitrova et al., 1999 ; Mahelka has been characterized using isozymes ( Werth, 1989 ) and DNA et al., 2005 ; Kron et al., 2007 ; Suda et al., 2007 ). Despite its ( Hutton, 1992 ), and its morphology has been extrapolated by potential taxonomic value, genome size has largely been ne- comparing its extant allotetraploid derivatives ( Werth and glected in the biosystematics of ferns in general (but see Bure š Kuhn, 1989 ; Fraser-Jenkins, 2001 ). The species are classifi ed in et al., 2003 ; Ebihara et al., 2005 ; Ekrt and Š tech, 2008 ; Ekrt the subgenus Dryopteris , section Lophodium (Newman) C. et al., 2009 ), and in the D. carthusiana group in particular. The Chr. ex H. It ô ( Fraser-Jenkins, 1986 ), which includes ferns with Plant DNA C-values database ( Bennett and Leitch, 2005 ) con- usually thick, glossy, and bicolor stipe-base scales, narrow tains only four estimates for the whole genus Dryopteris , in- lobes of ultimate segments, terminating in long, hair-tipped cluding the value for D. dilatata (1C = 8.05 pg), as determined aristate teeth, and unique spore morphology with minutely by Feulgen microdensitometry. spinulose surface on the perispore. Formerly, D. cristata (L.) A. In this study, we used relative genome size data together with Gray was also a part of the D. carthusiana group (e.g., Walker, analysis of multivariate morphometric data to obtain new in- 1955 , 1961 ; Wid é n et al., 1967 ). However, more recent treat- sights into phenotypic variation and the frequency of interspe- ments have placed D. cristata into the separate section Pandae cifi c hybridization in the D. carthusiana group in Central Fraser-Jenk. ( Fraser-Jenkins, 1986 ). Europe. Our investigation was inspired by the demonstration The characteristics of petiole scales and pinnule margins, that genome size is usually stable within the same taxonomic shape and color of the frond, and the presence and density of entity ( Greilhuber, 2005 ), while it often varies between differ- glandular hairs are some of the diagnostic characters used for ent taxa ( Bennett and Leitch, 2005 ). Consequently, genome species
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