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Home , Acanthaceae, Antirrhinum, Bacopa, Bignoniaceae, Boraginaceae, Buddlejaceae

Pat Reeves collecting water-starwort, verna. All photographs by R. Olmstead unless otherwise credited.

WHATEVER HAPPENED TO THE ? by Richard G. Olmstead

cience has been hard on some , and Hydrostachy, sbelonged that Callitriche might be closest to of our best-loved fami- phylogenetically, that is, were they the “scroph” genera Slies recently. Perhaps none part of the same branch of an evo- (snapdragon) and (fox- have been hit harder than the fig- lutionary lineage. Cronquist, whose glove), rather than near the mint wort , Scrophulariaceae. classification scheme dominated our family, , 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 , Callitriche, results from my indicated 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 , 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, (top left), and Mare’s-tail, (above), ceae, , , 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 . 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 (“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 , 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 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 ). 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 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 (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 . 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 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 as Pediculari s (lousewort), page 14). and Orthocarpu s(paint- For most of the 150 years since brush and ’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 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, , 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) ( ’s-beak) (b room-rape) ( owl’s clover) ( lousewort) Veronicaceae or Plantaginaceae ( or Plantain Family) Antirrhinum (snapdragon) Baco pa( water-hyssop) Callitriche( water-starwort) Co llinsia Digitalis (foxglove) (hedge-hyssop) Hippuris(m are’s-tale) (fluellin) Limo sella( mudwort) (toadflax) Mo havea (b eardtongue) ( plantain) Stemo dia Synthyris( kittentails) To nella Veronica( speedwell, brooklime) Scrophulariaceae (Figwort Family) includes () and ( butterfly bush) Myo porum Sc ro phularia(fi gwort) ( mullein) (monkey ) Unassigned (fa lse pimpernel)

18 FREMONTIA VOLUME 30:2, APRIL 2002 from the in ), or traits that are clearly uniquely derived, even if shared by some more distantly related family (pari- etal in Gesneriaceae; number reduced to two per carpel and each carpel divided by a “false septum” in Lamiaceae and Verbenaceae). However, the Scro- phulariaceae seem to be character- ized by unspecialized floral traits that may represent ancestral traits within the Lamiales. Even though work to sort out all of the details of evolutionary re- lationships within the Lamiales is continuing, a sufficiently robust pic- ture of relationships has emerged to enable us to identify major lin- eages suitable for recognition in a revised classification. The picture that emerges is one that shows some families mixed up with other fami- lies (e.g., Lamiaceae and - ceae), some families nested within other families (e.g., Myoporaceae and Buddlejaceae within Scrophu- lariaceae), and yet other families that are assemblages of unrelated lineages that will need to be dis- membered (e.g., and Scrophulariaceae). In some cases, adjusting the As a member of the genus that the family is named for, lance-leaved figwort, classification will mean little more lanceolata (above), remains in the Scrophulariaceae. Photograph by M. Denton. • Moth mullein, (below right), is still included in the Scrophulariaceae. sequenced, but the picture that I am that are five-parted, and superior about to describe of the demise of ovaries consisting of two fused car- the Scrophulariaceae has not been pels. Perhaps the most notable out- altered substantially by any of those lier in the group is the olive family results. (), which have four-parted Prior molecular systematic stud- flowers with two and ra- ies had determined that Cronquist’s dial symmetry. The atypical floral Scrophulariales and Lamiales (mi- morphology of the Oleaceae is not nus the ), along with so difficult to explain, considering the small orders Callitrichales and that its placement in the phyloge- Plantaginales, formed a monophyl- netic tree is at the very base of the etic group, all of which is now re- Lamiales. ferred to as Lamiales (Olmstead et Most of the families related to al. 1993). Flowers of plants in the the Scrophulariaceae can be identi- Lamiales tend to be pretty uniform fied by distinguishing traits that are in their appearance, typically hav- unique to the family (e.g., winged ing corollas with bilateral symme- seeds without in Big- try (often two-lipped, or bilabiate) noniaceae; retinacula for ejecting

VOLUME 30:2, APRIL 2002 FREMONTIA 19 than changing the rank of some encountered scroph. Both Scro phu- groups (e.g., family to subfamily or laria and Verbasc um belong to a vice versa), whereas in other cases, small group of genera within the new taxa will need to be named or Scrophulariaceae that is distributed named taxa will need to be altered in north temperate regions, mostly dramatically in their circumscrip- in . tion. In any event, the changes that Most of the rest of this family is are being made will be a test of in the southern hemisphere, par- how well the traditional Linnaean ticularly South , where four system of classification, which has tribes are endemic. has a served the taxonomic community substantial representation of the for 250 years, will hold up in the Scrophulariaceae in the form of the face of efforts to develop a new Myoporaceae, a group that is tradi- system of nomenclature (the tionally considered a distinct fam- method of applying names in a ily, but now is seen to belong nested classification, not the classifica- within the Scrophulariaceae. tion itself), but this is a subject for Buddlejaceae also is included in this another time! group and is distributed in Africa, The Scrophulariaceae, as tradi- Asia, and the . Exclud- tionally conceived, is worldwide in ing Myoporaceae and Buddlejaceae distribution and consists of approxi- from Scrophulariaceae would make mately 275 genera and over 5,000 the remaining group paraphyletic. species. The emerging classification Most North American botanists for the plants traditionally assigned think of Verbascum as an oddball to Scrophulariaceae will represent for the family due to its nearly radi- at least seven groups that will bear ally symmetric flowers. However, the rank of family. These will vary most of the Scrophulariaceae, as tremendously in size and several of we now define them, exhibit radial them will have a distinct geographic corolla symmetry, so it is Sc ro phu- focus. Some of these are newly laria, with its bilabiate corolla, that recognized (e.g., , is the real oddball. Buddlejaceae, Veronicaceae), while others repre- Myoporaceae, and most of the sent expansions of previously recog- South African scrophs all have co- nized families (e.g., Orobanchaceae, rollas that are radially symmetric, ). They are characterized or nearly so. as follows. Orobanchaceae. For many Scrophulariaceae. For those of years the Orobanchaceae have us here in the western US, the been accepted somewhat reluctantly Scrophulariaceae will become one as the bastard stepchild of the of those families that we will en- Scrophulariaceae. It was no secret counter on rare occasions in our that they were related to the scrophs native flora. Two genera native to and probably derived from them, , , in the but the distinctive suite of traits as- deserts of the southwest and , sociated with being an obligate para- and Scro phularia (figwort), are the site, or holoparasite, seemed suffi- only native genera that remain in cient to merit their own taxonomic this family; the , mullein (Ver- designation. bascum), will be our most frequently However, recent molecular sys-

Clustered broom-rape, (top), is included in the Orobanchaceae along with photosynthetic genera such as Pedicularis (louseworts). • Applegate Indian paintbrush, (middle). Paintbrushes are now included in the Orobanchaceae. Photograph by M. Denton. • English plantain, (bottom), is moved from the Plantaginaceae in the strict sense to a larger family, Plantaginaceae or Veronicaceae, which includes such genera as Antirrhinum (snap- dragons), Penstemon, and Veronica.

20 FREMONTIA VOLUME 30:2, APRIL 2002 Monkey flowers, such as the above Mimulus mephiticus from Yosemite National Park, are now placed in the Phyrmaceae. Photograph by C.S. Webber; its use courtesy of Jepson Herbarium, UC. tematic studies legitimize the Oro- curred multiple times within the de- several years ago, Callitric he and banchaceae and reunite them with scendants of that first parasitic spe- Hippuris (Olmstead et al. 2000). their rightful siblings, the green cies. Thus the traditional Oro- The third aquatic genus, Hydro- hemiparasites (capable of both pho- banchaceae, consisting of just the stachy,s is more closely related to tosynthesis and parasitism), includ- obligate parasites, is not a natural the hydrangeas and dogwoods than ing such well-known natives as the group without also including the it is to Callitriche and Hippuris louseworts (Pediculari),s Indian paint- hemiparasites with them. Conse- (Olmstead et al. 2000). brushes (Castilleja), and owl’s clo- quently, the Orobanchaceae now as- For this group, we have chosen vers (Castillejaan d Orthocarpu)s. Not sume a much more important a name calculated to create contro- only are all of the parasites (holo- role in the flora of western North versy. The International Code of and hemi-) united into a monophyl- America. requires etic group, thus providing the basis Veronicaceae. Many of our the use of the earliest validly pub- for their acceptance in our classifi- most familiar scrophs, including lished name for a family (or genus cation, they are not particularly close snapdragons (Antirrhinum), fox- or species) that is based on the name to any of the other major groups of glove (Digitalis), and such natives of a species included in the family. scrophs. Therefore, this is not sim- as , Penstemo,n and Veronica, We have chosen Veronicaceae, ply a matter of arbitrarily splitting belong to a third major lineage. which is the earliest validly pub- off a distinctive branch of a larger This group is worldwide in distri- lished name (1782) and one that Scrophulariaceae; these form a dis- bution and very diverse. Also in reflects its primary composition as tinct and distinctive lineage of plants. this group are several small groups former scrophs, to represent this The work of dePamphilis, often recognized as individual fami- newly recognized taxonomic group. Wolfe, and Young (dePamphilis et lies by virtue of having distinctive However, two rules conspire al. 1997; Wolfe & dePamphilis traits that obscure their true rela- against this choice. One is a nomen- 1997; Young et al. 1999) has shown tionships. These include Plantago clatural rule that permits excep- that parasitism in this group evolved (Plantaginaceae), (Glob- tions to strict priority, and allows only once. Perhaps more interest- ulariaceae), and two of the aquatic later names to be accepted or “con- ingly, they have shown that the loss genera mentioned in the beginning served” (in the lingo of taxonomic of and, therefore, the of this article that were the initial nomenclature). The second is an inability to photosynthesize, has oc- subject of the undergraduate thesis obscure rule in an appendix to the

VOLUME 30:2, APRIL 2002 FREMONTIA 21 Code of Nomenclature, which fur- cally, neither the name Mimulus, tion that will provide a much more ther constrains the choice of “con- nor any of the names of the other stable means of communicating our served” names to a starting date in small genera, have been published knowledge of many 1789. The Code requires that as the of a family name. There- generations into the future. Plantaginaceae be used for this fore, Phrymaceae has priority at the group. (Globulariaceae, Calli- rank of family for this group. By trichaceae, and Hippuridaceae all this point, you are probably cursing REFERENCES are preferred by the Code over any out loud. But, bear up—you’ve just other name, too, but occur later learned a new family! dePamphilis, C.W., N.D. Young, and than Plantaginaceae.) Are there yet more families? A.D. Wolfe. 1997. Evolution of The international committee Yes. But these are ones that you gene rps2 in a lineage of charged with settling disputes about won’t encounter here in the wilds hemiparasitic and holoparasitic nomenclature rejected our request of the western US. A pretty orna- plants: Many losses of photosyn- thesis and complex patterns of rate to use any name other than Plan- mental plant, with which many of variation. Proceedings of the National taginaceae. However, given that you may be familiar, Calceo laria Academy of Scienc 94es :7367–7372. Plantaginaceae already is identified (pocket-book plant), along with two Olmstead, R.G., B. Bremer, K. Scott, with a well-known and monophyl- small genera native to South and J.D. Palmer. 1993. A parsimony etic group, and recognizing the in- America and , are analysis of the Asteridae lato advisability of forcing the many new isolated from all other scrophs and based on rb cL sequences. Annals o f groups being recognized today to comprise a new family, Calceo- the Missouri Bo tanical Gard e80:n fit into a few Linnaean ranks, we lariaceae (not just new to us pro- 700–722. have chosen to ignore the Code and vincial botanists here in the west- Olmstead, R.G. and P.A. Reeves. 1995. name this group Veronicaceae. ern US, but a newly-described Evidence for the of the Phrymaceae. If you have stud- family). In , a few Scrophulariaceae based on chloro- plast rb cL and ndhF sequences. An- ied primarily in the western former scroph genera were found nals o f the Misso uri Bo tanical Garden US, chances are you have not heard to be related to a group called the 82:176–193. of this family. As presently con- Stilbaceae and are transferred to Olmstead, R.G., R.K. Jansen, K.-J. ceived, it includes a single genus, that family. Lastly, (em- Kim, and S.J. Wagstaff. 2000. The Phryma, which has either one or press tree), a group of six species phylogeny of the Asteridae s.l. based two species, depending on whether of large from China with on chloroplast ndhF sequences. east Asian and eastern North Ameri- showy flowers reminiscent of Cat- Mo lecular and Evo lutio n can populations are considered alpa and sometimes placed in the 16:96–112. separate species or not. The plants Scrophulariaceae, are isolated from Olmstead, R.G., C.W. dePamphilis, are small, perennial, understory any of the other families and are A.D. Wolfe, N.D. Young, W.J. in with tiny, best considered their own family, Elisens, and P.A. Reeves. 2001. Dis- primarily self-pollinating flowers. . integration of the Scrophulariaceae. The flowers have unusually long As scientists, we plant taxono- Americ an Jo urnal o f Bo tan 88:y 348– 361. curled tips on the calyx and a single- mists consider ourselves fortunate Wolfe, A.D. and C.W. dePamphilis. seeded fruit, which accounts for to be a part of what is one of the 1997. Alternate paths of evolution their isolated taxonomic position. eras of greatest advancement in our for the photosynthetic gene rb cL in However, if you look closely you field since the tremendous age of four nonphotosynthetic species of can see a little monkey face smiling discovery in the 18th and 19th cen- Orobanch.e Plant Mo lecular Bio lo gy back at you. turies. At the same time we recog- 33:965–977. The doctoral research of Paul nize the fact that many botanists of Young, N.D., K.E. Steiner, and C.W. Beardsley at the University of our generation, amateur and pro- dePamphilis. 1999. The evolution of Washington has shown that Phryma fessional alike, may find the changes parasitism in the Scrophulariaceae/ is, in fact, a monkey flower and is in plant classification confusing and Orobanchaceae: Plastid gene se- evolutionarily derived from ances- even counterproductive to the pur- quences refute an evolutionary tran- tors that we would call Mimulus pose of communicating about sition series. Annals of the Missouri were we to encounter them today. biodiversity. However, if our classi- Botanical Garde n86:876–893. Phryma, Mimulus, and six to eight fication is to truly represent the pat- other small genera comprise a tern of biodiversity stemming from Richard G. Olmstead, Department of monophyletic group that is not the evolutionary history of the Bo tany, Campus Bo x 355325, University closely related to any of the other plants on earth today, changes we o f Washingto n, Seattle, WA 98195. groups of former scrophs. Ironi- make now will result in a classifica- [email protected]

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