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Evolutionary Changes in Floral Structure Within Lepidium L

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Evolutionary Changes in Floral Structure Within Lepidium L Int. J. Plant Sci. 160(5):917±929. 1999. q 1999 by The University of Chicago. All rights reserved. 1058-5893/1999/16005-0013$03.00 EVOLUTIONARY CHANGES IN FLORAL STRUCTURE WITHIN LEPIDIUM L. (BRASSICACEAE) John L. Bowman,1,* Holger BruÈggemann,² Ji-Young Lee,* and Klaus Mummenhoff² *Section of Plant Biology, University of California, Davis, California 95616, U.S.A.; and ²UniversitaÈt OsnabruÈck, Fachbereich Biologie, Spezielle Botanik, Barbarastrasse 11, 49069 OsnabruÈck, Germany The basic ¯oral ground plan is remarkably constant across Brassicaceae. However, within Lepidium (ca. 175 species), deviations from this ground plan are common, with over half of Lepidium species having only two stamens rather than the usual six and a further eighth of the species having only four stamens. Furthermore, petals are reduced in size in a majority of Lepidium species. In order to determine the frequency and direction of changes in ¯oral structure within Lepidium, we have inferred the phylogeny within the genus from sequences of the internal transcribed spacers of the nuclear ribosomal DNA. On the basis of this inferred phylogeny, we conclude that ¯oral structure within Lepidium is relatively ¯uid. In order to account for the phylogenetic distributions of the different ¯oral ground plans, at least two independent reductions to the two-stamen condition and at least one reversal to ¯owers with increased organ numbers are likely to have occurred. To account for the frequency of morphological evolution observed within the genus, we propose that some clades within Lepidium may be predisposed to changes in ¯oral structure. In addition, several transoceanic dispersals are needed to explain the geographic distributions of the clades inferred from the phylogeny. Keywords: Lepidium, ¯ower structure, ¯ower evolution, internal transcribed spacers, Brassicaceae. Introduction rudimentary in many others. Thus, the basic ground plan of Brassicaceae is found in less than half of the Lepidium species. While ¯oral structure varies greatly among angiosperms as Lepidium has a widespread distribution, with species en- a whole, at lower taxonomic levels ¯oral structure is usually demic to all continents (with the exception of Antarctica) and highly conserved. This conservation suggests that ¯oral struc- many oceanic islands, such as New Zealand and Hawaii. Thel- ture is under strict genetic control. One approach to under- lung (1906) classi®ed species of Lepidium into seven sections. standing the genetic control of ¯oral ground plans is to analyze In this classi®cation made on the basis of morphological fruit patterns in ¯oral ground plan variation between closely related characters, most of the species with two stamens were placed species. This approach assumes that the differences between in the section Dileptium, whose distribution includes all in- species arise from the ®xation of relatively few genetic deter- habited continents. Likewise, species with four medial stamens minants. Brassicaceae provide a tractable model because the are found in North and South America and Australia. These ¯oral ground plan is remarkably conserved among the family's distributions suggest that there have been independent parallel more than 3000 species in ca. 350 genera (Schulz 1936; Cron- reductions in ¯oral ground plan on several continents, or that quist 1981; Endress 1992). The stereotypical Brassicaceae there have been multiple intercontinental migrations, or a com- ¯ower consists of four sepals, four petals, six stamens, and bination of both. To resolve this issue we have inferred the two carpels. The six stamens are arranged so that four are phylogenetic relationships of species within the genus Le- in medial positions and two are in lateral positions within the pidium from sequences of the internal transcribed spacers (ITS) ¯ower. While deviations from this basic ground plan are of the nuclear ribosomal DNA. These sequences have been rare within Brassicaceae as a whole (for review, see Endress shown to be very useful for resolving phylogenetic relation- 1992), reductions in ¯oral organ numbers are common within ships within and among plant genera (reviewed in Baldwin et the genus Lepidium, which consists of ca. 175 species (®g. 1; al. 1995). The results indicate that there have been at least Thellung 1906; Hewson 1981; Al-Shehbaz 1986; Rollins two independent reductions in ¯oral ground plan, and one or 1993). Stamens are reduced from six to two in ca. one-half of more reversals to increased ¯oral organ number. Our results the species, while a further one-eighth have only four stamens further suggest that multiple transoceanic migrations have (Al-Shehbaz 1986). In the case of species with two stamens, occurred. stamens develop in medial positions only. Species with four stamens can have four medial stamens or two lateral and two medial stamens. In addition, petals are reportedly absent from ca. one-quarter of the Lepidium species, and they are Material and Methods On the basis of phylogenies constructed from ca. 100 Le- 1 Author for correspondence and reprints; e-mail jlbowman@ pidium species analyzed (H. BruÈ ggemann and K. Mummen- ucdavis.edu. hoff, unpublished data), a critical assemblage of Lepidium spe- Manuscript received March 1999; revised manuscript received June 1999. cies was chosen to re¯ect changes that have occurred in ¯oral 917 918 INTERNATIONAL JOURNAL OF PLANT SCIENCES Fig. 1 Floral structure. A, Lepidium phlebopetalum (2 lateral 1 4 medial stamens); B, Lepidium perfoliatum (2 1 4); C, Lepidium vesicarium (2 1 4); D, Lepidium graminifolium (2 1 4); E, Lepidium africanum (0 1 2); F, Lepidium hyssopifolium (0 1 2); G, Lepidium oleraceum (2 1 2); H, Lepidium lasiocarpum (0 1 2); I, Lepidium virginicum (0 1 2); J, Lepidium fremontii (2 1 4); K, Lepidium dictyotum (0 1 4); L, Lepidium oxytrichum (0 1 4); M, Lepidium fasciculatum (0 1 2); N, Lepidium ruderale (012); O, Lepidium sativum (2 1 4). One sepal has been removed in E and M, and two sepals have been removed in K. BOWMAN ET AL.ÐEVOLUTION OF LEPIDIUM FLOWER STRUCTURE 919 ground plan. This assemblage was chosen for several reasons. replicates was performed saving no more than 300 trees per First, the present taxon sample represents a broad spectrum replicate to obtain estimates of reliability for each monophy- of the variation in Lepidium including members of six (out of letic group. The sequences were also analyzed using a maxi- seven) sections and 11 (out of 11) greges sensu Thellung mum likelihood search with the values for ti/tv and g distri- (1906). Second, these species re¯ect all types of changes that bution (with four rate categories) estimated from the 15 most have occurred in ¯oral ground plan. Third, the ratio of the parsimonious trees. A single tree was found after 10 random distribution patterns of the different ¯ower types within each taxon addition replicates, starting with the 15 most parsi- clade corresponds to the ratio in the phylogenies constructed monious trees, using the Hasegawa-Kishino-Yano model of using ca. 100 Lepidium species. Thus, ancestral character state sequence evolution (Hasegawa et al. 1985). reconstruction on this critical assemblage should re¯ect that Ancestral state reconstruction was performed on the 15 most which was supported by sampling the full 100 species data parsimonious trees using the parsimony, Acctran, and Deltran set. Collection data and sources of plant material for obtaining options on MacClade 3.07 (Maddison and Maddison 1992), ITS sequences are presented in table 1. with the exception of one tree in which a four-clade polytomy Because Lepidium may not clearly be separated from closest existed; this tree was analyzed using only the parsimony op- related genera, i.e., Cardaria (treated by Thellung as a section tion. The most parsimonious trees suggest that the character of Lepidium), Coronopus, Stroganowia, and Andrzeiowskia state of two stamens has evolved multiple times. To test the (all from subtribe Lepidiinae, tribe Lepidieae), we used the robustness of this conclusion, we constrained the topology to outgroup species, Hornungia alpina (L.) O. Appel and Hor- group the two-stamen species in a single clade by joining node nungia procumbens (L.) Hayek (Appel and Al-Shehbaz 1997). 10 with either node 5 or node 7. MacClade 3.07 was used to In a recent chloroplast DNA analysis of tribe Lepidieae (K. determine the length of resultant shortest trees. Complete re- Zunk, K. Mummenhoff, and H. Hurka, unpublished data). Hornungia is sister to the Lepidium/Cardaria/Coronopus arrangement searches above and below the branch leading to clade. the single two-stamen clade in both of the arti®cial trees were Fresh or dry leaves (from herbarium specimens) were taken performed to discover the shortest possible topology given this from individual plants. Total DNA was isolated following constraint. To assess whether this constrained topology was the procedure of Doyle and Doyle (1987). Double stranded signi®cantly worse than the shortest trees recovered without DNA of the ITS-1 and ITS-2 regions was ampli®ed using the this constraint, a series of nonparametric tests was conducted polymerase chain reaction (PCR) protocol given in Mum- using PAUP 4.0b1. Tree length was used as an evaluation cri- menhoff et al. (1997). Primer 18 F was modi®ed as described terion for these tests. Twenty-®ve thousand trees were gener- in Mummenhoff et al. (1997, ®g. 1). Ampli®cation products ated through a heuristic search of the ITS dataset, and all trees were puri®ed using the Qiaquick PCR Puri®cation Kit (Qia- ·10 steps longer than the shortest trees were saved. A series gen, Hilden, Germany). Puri®ed DNAs were sequenced by of tree ®lters was used to segregate trees into ®les containing the dideoxy chain termination method (Sanger et al. 1977) 30 trees of the shortest length, one step longer than the shortest using the fmol kit (Serva, Heidelberg), following the protocol trees, two steps longer than the shortest trees, and so on.
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