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Biosystematic Analysis of the Cystopteris

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Biosystematic Analysis of the Cystopteris BIOSYSTEMATIC ChristopherH. Haufier,2 MichaelD. Windham2'3and ANALYSIS OF Thomas A. Ranker4 THE CYSTOPTERIS TENNESSEENSIS (DRYOPTERIDACEAE) COMPLEX' ABSTRACT The allotetraploid Cystopteris tennesseensis and its putative diploid progenitors, C. bulbifera and C. protrusa, constitute the C. tennesseensis complex. Although previous studies provided evidence of morphological, ecological, and chromosomal differences among the members of this complex, puzzling morphological variability precluded consistent identification and treatment of the taxa. The current study combined morphometric analyses with surveys of chromosomal, isozymic, and gametophytic features and supported past treatments of the complex as three separate species. The diploids shared no allozymes for the nine enzymes examined, and meiotic analyses of triploid hybrids with C. tennesseensis provided additional evidence that the diploid genomes are nonhomologous. Because C. tennes- seensis has a relatively narrow range and contains isozymic profiles that are consistently additive of diploid patterns, we suggest that this allopolyploid is a relatively young species. Isozymic variation in the tetraploid parallels that observed in the diploids, implying that genetic variability was introduced through recurrent hybridization. Analyses of isozymic data and gametophytic features indicated that the diploids outcross frequently and thus may form hybrids readily when sympatric with the tetraploid. In part because of these characteristics, precise identification of species and hybrids in this complex is difficult and depends on evaluation of cryptic features. The cosmopolitan genus Cystopteris Bernh. has directed into teeth were placed in sect. Cystopteris, been called "perhaps the most formidable biosys- while those with veins directed into sinuses were tematic problem in the ferns" (Lovis, 1977, p. assigned to sect. Emarginatae. Blasdell encoun- 356). Although Cystopteris species are primarily tered variability for this vein termination character north temperate and therefore readily accessible in some specimens and suggested that such anom- to pteridologists, complex patterns of morpholog- alies could result from introgression. Lovis (1977), ical variation have thwarted satisfactory taxonomic on the other hand, considered it more likely that treatments. The most recent monograph (Blasdell, venation features are not as stable in some species 1963) recognized ten species in two subgenera. as in others and should not be used to define sec- Subgenus Acystopteris includes the Asian species tions. C. japonica and C. tenuisecta, which are so dis- Our observations suggested that Lovis was cor- tinctive that some have placed them in a separate rect and, rather than organizing the North Amer- genus (Nakai, 1933; Pichi-Sermolli, 1977). Blas- ican Cystopteris species into morphologicallybased dell divided the remaining species (all in subg. Cys- sections, we have chosen to concentrate on inter- topteris) into two sections based on the pattern of active species complexes involving allopolyploid vein terminationin the leaves. Species having veins species and their putative diploid progenitors. One I CHH is profoundly indebted to Alice and Rolla Tryon for providing the opportunity through a Gray Herbarium Postdoctoral Fellowshipto delve deeply into the world of ferns and for passing on by example their infectious curiosity about these marvelous plants. This research was supported by the National Science Foundation. We thank Donald Burke, Cara Burres, Lori Hanson, Warren Hauk, Carol Kuhn, Robin Prentice, and Eric Rabe for technical assistance, David Barringtonfor drawing Figure 1, and the officers of the following herbaria for loans of specimens: COLO, DAO, GH, ILLS, IND, KANU, KE, KY, MICH, MIL, MO, NY, PAG, OAC, OS, SIU, TENN, UARK, US, VPI, VT, and WIS. We are especially thankful to Ralph Brooks and Ron McGregor of KANU for housing the many hundreds of specimens. Living specimens were generously supplied by D. M. Britton, R. E. Brooks, S. C. Churchill, J. J. Doyle, R. C. Moran, T. Reeves, D. E. Soltis, W. C. Taylor, C. K. Teale, and W. H. Wagner. 2 Department of Botany, University of Kansas, Lawrence, Kansas 66045, U.S.A. 3Present Address: Utah Museum of Natural History, University of Utah, Salt Lake City, Utah 84112, U.S.A. 4University of Hawaii, Hawaiian Evolutionary Biology Program, Honolulu, Hawaii 96822, U.S.A. ANN. MISSOURIBOT. GARD. 77: 314-329. 1990. This content downloaded from 129.237.46.100 on Thu, 11 Sep 2014 14:45:22 PM All use subject to JSTOR Terms and Conditions Volume 77, Number 2 Haufler et al. 315 1990 Analysis of the Cystopteris tennesseensis Complex such complex centers on C. tennesseensis, a species TABLE 1. Mean spore sizes and standard deviations first recognized by Shaver (1950) who described calculated by measuring the long axis of 25 spores. Spec- it as a hybrid between C. bulbifera and C. protrusa. imens whose ploidy level has been verified by meiotic chromosome squashes are indicated by asterisks. States In 1954 Shaver developed an extended discussion listed in parentheses are those from which the specimens of the morphology and ecology of the complex were collected. which still stands as an excellent summary of the natural history of this difficult group. C. bulbifera (Illinois) 37.48 ? 1.949 From the moment it was named, there was dis- C. bulbifera* (Oklahoma) 35.21 ? 3.408 agreement concerning the proper status and dis- C. bulbifera* (Arizona) 36.27 ? 2.560 position of C. tennesseensis. McGregor (1950), in C. bulbifera* (Indiana) 35.96 ? 2.325 collaboration with C. A. Weatherby, reduced this C. bulbifera* (Ohio) 39.81 ? 2.944 species to a variety of C. fragilis. In addition, C. bulbifera (Ohio) 35.71 ? 3.038 citing specimens that did not conform to the pro- C. bulbifera (Kentucky) 34.39 ? 1.764 tologue of C. fragilis var. tennesseensis and that C. bulbifera (Indiana) 36.78 ? 2.336 seemed to be close to Weatherby's C. fragilis f. mean= 36.45 ? 1.650 simulans, McGregor recognized C. fragilis var. C. protrusa (Illinois) 33.65 ? 1.788 simulans. This approach seemed justified because C. protrusa* (Kansas) 35.22 ? 4.714 some specimens tend to bridge the morphological C. protrusa (Missouri) 33.33 ? 2.421 gap between these two varieties as well as between C. protrusa* (Kansas) 30.77 ? 1.868 C. fragilis var. fragilis and C. fragilis var. ten- C. protrusa* (Kansas) 30.98 ? 2.260 C. protrusa* (Michigan) 33.21 ? 2.332 nesseensis. However, Blasdell (1963) revealed C. C. protrusa* (North Carolina) 34.22 ? 3.042 tennesseensis as a tetraploid with n = 84 chro- mean= 33.05 ? 1.634 mosomes. His analysis showed that hybridization between C. protrusa and C. bulbifera was the most C. tennesseensis* (Kansas) 40.02 ? 3.250 reasonable explanation for the origin of this tet- C. tennesseensis* (Missouri) 41.40 ? 1.907 raploid. Therefore, Blasdell resurrected C. tennes- C. tennesseensis* (Illinois) 41.29 ? 2.416 C. tennesseensis* 40.65 ? 2.084 seensis as a species, including the former C. fra- (Arkansas) gilis var. simulans. mean = 40.84 ? 0.639 The subtlety of morphological features separat- ing the species as well as the continued discovery of intermediates has perpetuated the systematic confusion of the C. tennesseensis complex. Even butional information. When the gross morphology though the accumulated data demonstrate conclu- of specimens was not sufficient to assign them readi- sively that C. tennesseensis is isolated from its ly to species, spores were removed and mounted congeners, this tetraploid has not been widely ac- in Permount on glass microscope slides. The longest cepted as a distinct species. As recently as 1982, diameter of the monolete spores (Table 1) and Moran (1982, p. 94) found in a study of Cystop- evidence of abortion (e.g., shrunken or malformed teris specimens from Illinois that "all 90 herbarium spores) was noted. Spore slides were placed in en- specimens of C. tennesseensis . .. were originally velopes and attached to herbarium sheets. misidentified." To supplement herbarium collections and supply In this paper, we report a series of analyses living material for chromosomal, isozymic, and designed to investigate the patterns and the pro- common garden morphological comparisons, spec- cesses behind the systematic confusion in C. ten- imens were collected over much of the range of nesseensis. We describe studies of biogeography, the genus in North America and were donated as morphology, chromosomes, and isozymes that clar- noted in footnote 1. Living collections were main- ify the origin and current status of C. tennesseensis tained in the University of Kansas greenhouses. and its progenitor diploids. Collection sites for materials used in this study are listed in Table 2. Ecologically induced morphological variation may MATERIALS AND METHODS obscure genetically based species distinctions. Observations of morphological variability, geo- Therefore, we conducted discriminant analyses of graphic distribution, and habitat diversity were ob- morphological variation based on plants cultivated tained from surveys of herbarium specimens. If in the greenhouse. All individual plants were iden- specific locality data were supplied, collection sites tified and assigned to a group on the basis of chro- were plotted by county and used to obtain distri- mosome number and isozymic composition. Fea- This content downloaded from 129.237.46.100 on Thu, 11 Sep 2014 14:45:22 PM All use subject to JSTOR Terms and Conditions 316 Annals of the Missouri Botanical Garden TABLE
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