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WHATEVER HAPPENED to the SCROPHULARIACEAE? by Richard G

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WHATEVER HAPPENED to the SCROPHULARIACEAE? by Richard G Pat Reeves collecting water-starwort, Callitriche verna. All photographs by R. Olmstead unless otherwise credited. WHATEVER HAPPENED TO THE SCROPHULARIACEAE? by Richard G. Olmstead cience has been hard on some Hippuris, and Hydrostachy, sbelonged that Callitriche might be closest to of our best-loved plant fami- phylogenetically, that is, were they the “scroph” genera Antirrhinum Slies recently. Perhaps none part of the same branch of an evo- (snapdragon) and Digitalis (fox- have been hit harder than the fig- lutionary lineage. Cronquist, whose glove), rather than near the mint wort family, Scrophulariaceae. classification scheme dominated our family, Lamiaceae, as others had My interest in the Scrophu- views of plant relationships for the thought. I suggested to Pat that he lariaceae started innocently enough last 30 years of the 20th century, should sample a number of other when an undergraduate student assigned each of these genera to its representatives of the Scrophu- working in my lab, Pat Reeves, de- own family and all three to the or- lariaceae, as well as some other cided to look to see where three der Callitrichales. Some preliminary members of Cronquist’s orders genera of aquatic plants, Callitriche, results from my research indicated Lamiales and Scrophulariales. VOLUME 30:2, APRIL 2002 FREMONTIA 13 The very first results seemed to indicate that something was amiss. Two groups of genera, normally assigned to Scrophulariaceae, seemed to form distinct branches on the resulting evolutionary tree, but did not come out together. While we could not be confident of the relationships among all the families included in that study, we were confident that these two groups of genera were as distant from each other as any of several major families in this part of the “tree of life” were from each other, including the Lamiaceae, Acantha- Water-starwort, Callitriche verna (top left), and Mare’s-tail, Hippuris vulgaris (above), ceae, Bignoniaceae, Verbenaceae, are now included in the Veronicaceae. TREE OF LIFE he metaphor of the “tree of life” has been used ever since Darwin’s time to conceptualize the pattern of Trelationships among species. A classification that reflects the tree of life would be hierarchical in nature, with branch tips representing species and the branches themselves representing groups in the classification. Our present system of classification consists of a series of ever-more-inclusive ranks. Closely related species make up a genus (“twig” on the tree metaphor), one or more genera make up a family (larger branch), and so on down the tree towards the “trunk” with order, class, phylum, and kingdom. In order for the resulting classification to accurately reflect the evolutionary relationships or phylogeny, each named group in the classification must connect to the rest of the tree at a single point (or “saw cut,” if we are pruning the “tree”). Each such group is termed monophylet i(lciterally “one branch”), whereas groups that consist of two or more branches pruned separately from the tree are termed polyphylet.Tic hose that require one cut to prune a branch, but then another cut to exclude one of the smaller branches from that branch are termed paraphyletic Tr. aditional classifications are largely monophyletic, but typically have some polyphyletic groups and many paraphyletic groups. 14 FREMONTIA VOLUME 30:2, APRIL 2002 DNA SEQUENCES ost of the evidence for plant evolutionary relationships in recent years has come from a comparison of Mthe DNA sequences of various genes, usually those found in the chloroplast of the plant cell. A single gene, or even three genes as used in the study on which this article is based, are but a small fraction of the entire genetic material in a plant (its genome). However, the variation in DNA sequences for even a gene of modest length—for example 1,000 nucleotides long—is likely to have more information about evolutionary relationships than the anatomy and morphology on which traditional classifications are based. It is also easier to compare using new computer analyses. In the study of Olmstead et al. (2001), three genes totaling more than 4,200 nucleotides were compared for 65 species of plants in the Scrophulariaceae and related families. and Gesneriaceae (Olmstead and sity—Claude dePamphilis, Andrea Reeves 1995). Ever since Darwin Wolfe, and Ned Young, who were said that classification should be studying the parasitic members of “genealogical,” taxonomists have the Scrophulariaceae and Oroban- tried their best to continually re- chaceae—to better understand the vise classifications to reflect the origin and evolution of parasitism. natural order of evolutionary rela- (Parasitism in this case is the ability tionships, the pattern we call phy- to develop the parasitic connections lo geny today. A classification that called haustoria to the roots of other reflects phylogeny would be one in plants.) which all of the species assigned to In Pat’s study, we had not a given group—whether a genus, sampled any of the parasitic scrophs, family, or any other group we may not wanting to interfere with their want to name—share a more re- research. However, Claude, Andi, cent common ancestor with each and Ned had some tantalizing evi- other than with any species outside dence that the parasites, including the group. This is what is called a such well known western wild- monophyletic group (see sidebar on flowers as Pediculari s (lousewort), page 14). Castilleja and Orthocarpu s(paint- For most of the 150 years since brush and owl’s clover), and Darwin’s ideas transformed the way Orobanch (be room-rape), all formed we think about living things, the a closely related group of plants that changes in our classifications have was not close to either of the two come gradually. However, the pace groups we had identified. of change has picked up dramati- As fate would have it, our two cally in recent years due to the com- labs had only a partially overlapping bined effect of new, more rigorous set of DNA sequences, so we un- ways of assessing phylogenetic re- dertook the job of backtracking and lationships and the tremendous in- obtaining all of the DNA sequence The genus Castilleja (purple owl’s-clover, flux of data from DNA sequences data we would need for all of the C. exserta, shown here) is now included in the Orobanchaceae family along with (see sidebar above). species we had sampled. We also broom-rapes and louseworts. Photograph That first study was modest in added some more species to the list by J. Vale; its use courtesy of Jepson scope: after all, it was an under- to try to sample as many of the tribes Herbarium, UC. graduate thesis project! I knew that (rank more inclusive than genus, but I would have to dramatically in- smaller than family) of Scrophu- al. 2001). Our data consisted of crease the sampling in order to nail lariaceae as possible from around DNA sequences for three genes and down the extent to which changes the world. In all, we sampled 39 totaled more than 4,200 nucleotides would need to be made in our clas- genera of scrophs, representing 24 of DNA. Since the body of evidence sification of the Scrophulariaceae. tribes, along with representatives of for this study was obtained, numer- At this point I contacted a group of 15 closely related families for a re- ous other species have been sampled researchers at Vanderbilt Univer- cently published study (Olmstead et and additional genes have been VOLUME 30:2, APRIL 2002 FREMONTIA 15 Figure 1. This tree represents the consensus relationships based on the DNA sequences of two genes from the chloroplast genome. Areas of uncertainty regarding relationships are indicated by the unresolved nodes on the tree. Numbers on the branches represent 16 FREMONTIA VOLUME 30:2, APRIL 2002 bootstrap values (scale 0 - 100) which provide a relative measure of support for individual branches. The names on the right in bold are the names of the major groups (indicated by brackets) recognized in our study, while those in parentheses with arrows indicate former family placement of some genera. VOLUME 30:2, APRIL 2002 FREMONTIA 17 TABLE 1. GENERA INCLUDED IN CALLITRICHACEAE, HIPPURIDACEAE, OROBANCHACEAE, PLANTAGINACEAE, AND SCROPHULARIACEAE IN THE JEPSON MANUAL (1993) WITH THEIR NEW FAMILY ASSIGNMENTS Orobanchaceae (Broom-rape Family) Bellardia Bo schniakia( ground-cone) Castilleja( Indian paintbrush, owl’s clover) Cordylanthus( bird’s-beak) Orobanche(b room-rape) Orthocarpus( owl’s clover) Parentucellia Pedicularis( lousewort) Triphysaria Veronicaceae or Plantaginaceae (Veronica or Plantain Family) Antirrhinum (snapdragon) Baco pa( water-hyssop) Callitriche( water-starwort) Co llinsia Cymbalaria Digitalis (foxglove) Dopatrium Galvezia Gratiola (hedge-hyssop) Hebe Hippuris(m are’s-tale) Keckiella Kickxia (fluellin) Limo sella( mudwort) Linaria (toadflax) Maurandya Mo havea Nothochelone Penstemon(b eardtongue) Plantago( plantain) Stemo dia Synthyris( kittentails) To nella Veronica( speedwell, brooklime) Scrophulariaceae (Figwort Family) includes Buddlejaceae (Loganiaceae) and Myoporaceae Buddleja( butterfly bush) Myo porum Sc ro phularia(fi gwort) Verbascum( mullein) Phrymaceae Mimulus (monkey flower) Unassigned Lindernia(fa lse pimpernel) 18 FREMONTIA VOLUME 30:2, APRIL 2002 seeds from the fruit in Acanthaceae), or traits that are clearly uniquely derived, even if shared by some more distantly related family (pari- etal placentation in Gesneriaceae; ovule number reduced to two per carpel and each carpel divided by a “false septum” in Lamiaceae
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