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Home , Aetheorhiza, Dendroseris, Dendroseris litoralis, Macaronesia, Prenanthes, Sonchus

Proc. Natl. Acad. Sci. USA Vol. 93, pp. 7743-7748, July 1996 Evolution

A common origin for woody and five related genera in the Macaronesian islands: Molecular evidence for extensive radiation (adaptive radiation/molecular evolution/biogeography) SEUNG-CHUL KIM*, DANIEL J. CRAWFORD*t, JAVIER FRANCISCO-ORTEGAt, AND ARNOLDO SANTOS-GUERRA§ *Department of Biology, Ohio State University, Columbus, OH 43210-1293; tDepartment of Botany, The University of Texas, Austin, TX 78713-7640; and 3Jardin de Aclimataci6n de La Orotava, 38400 Puerto de La Cruz, , , Communicated by Michael T. Clegg, University of California, Riverside, CA, March 15, 1996 (received for review January 4, 1996)

ABSTRACT Woody Sonchus and five related genera (Bab- agules to the islands is a very rare event. This in turn makes it cockia, Taeckholmia, Sventenia, Lactucosonchus, and Prenan- more likely that related endemics on remote archipelagos have thes) of the Macaronesian islands have been regarded as an a common origin, i.e., represent a monophyletic group. Unlike outstanding example of adaptive radiation in angiosperms. more remote volcanic islands in the Pacific (Juan Fernandez, Internal transcribed spacer region of the nuclear rDNA (ITS) Hawaiian, and Galapagos Islands) where most evolutionary sequences were used to demonstrate that, despite the extensive studies of insular endemic have been carried out, the morphological and ecological diversity ofthe plants, the entire Macaronesian islands (Fig. 1) are very close to possible source alliance in insular Macaronesia has a common origin. The areas and exhibit a broad range of geological ages (17-22). (In sequence data place Lactucosonchus as sister group to the this paper, "Macaronesian" will refer to the islands of this area, remainder of the alliance and also indicate that four related and the Canary Islands will be specified when referring to that genera are in turn sister groups to subg. Dendrosonchus and archipelago alone.) The proximity of the islands to the African Taeckholmia. This implies that the woody members ofSonchus continent and their different geological ages make it much were derived from an ancestor similar to allied genera now more likely that multiple colonization events could have present on the Canary Islands. It is also evident that the occurred for some closely related taxonomic groups and that alliance probably occurred in the Canary Islands during the some taxa could be much older than others. This means, of late Miocene or early Pliocene. A rapid radiation of major course, that closely related endemic taxa may not be mono- lineages in the alliance is consistent with an unresolved phyletic. There also has been a long controversy over whether polytomy near the base and low ITS sequence divergence. some of the woody Macaronesian endemics are relict elements Increase of woodiness is concordant with other insular en- of a flora that extended along the during demics and refutes the relictural nature of woody Sonchus in the Tertiary period or are recent derivatives from continental the Macaronesian islands. ancestors (3, 6, 17, 23-26). There are 34 taxa of ca. 130 taxa in the subtribe Sonchinae Ascertaining the origin and evolution of plants endemic to () endemic to Macaronesia (27), with most of them oceanic islands is both fascinating and frustrating. Endemics in the Canary Islands. A previous phylogenetic analysis of the may assume the typical insular woody habit and become very Sonchinae (ref. 28; Fig. 2) recognized a Macaronesian clade distinct in other suites of characters such that determining that includes the woody members of Sonchus and five related their continental relatives is difficult if not impossible with genera (hereafter for convenience often referred to as the morphology (1-4). Once a colonizer becomes established on woody Sonchus alliance), but this was based on limited taxon an oceanic island, extensive diversification may occur as plants sampling from Macaronesia. This alliance is composed pri- move into a variety of open . This process has been marily of 19 species of woody Sonchus (i.e., subg. Dendroson- viewed as a good example of adaptive radiation (2-9), and once chus), the genera Babcockia, Taeckholmia, Sventenia, Lactu- it occurs, the different descendent lines may exhibit a wide cosonchus, one species of Sonchus subg. Sonchus (i.e., S. array of characters, making it difficult to determine whether tuberifer), and one species of . Two taxa, Lactu- they evolved from a common ancestor. Thus, difficult prob- cosonchus and S. tuberifer, are the only members of the group lems posed by insular endemics include whether they result that do not have a true woody habit; they are herbaceous from a single introduction, estimating the time of radiation, perennials with tuberous . As may be inferred by the and identifying the continental relative(s) and source area(s) recognition of six genera, these taxa display great morpholog- of the original colonizer(s) (10-12). As noted above, compar- ical, ecological, and anatomical diversity (29, 30). Despite this ative morphology may be of limited value for addressing these diversity, the fertility of several intergeneric hybrids suggests questions because of the difficulty in distinguishing features genetic cohesiveness within the alliance (31, 32). The basic shared by common ancestry as opposed to parallelisms. Mo- question is whether this remarkable array ofplants results from lecular sequences, however, have proven useful in the study of a single introduction followed by extensive radiation and some insular groups because, contrasted with morphology, diversification or from several introductions from nearby and base substitutions of determined regions (mutations) may be closely related source areas over a long period of time. It has neutral or nearly so (11, 13-16). been shown, for example, that the three genera of the very One of the basic assumptions in the study of the origin and diverse silversword alliance in the Hawaiian Islands came from evolution of endemics in oceanic islands is that the remoteness a single dispersal event (10, 33), but the extreme isolation of of the islands from possible source areas (combined with their small land masses) acts like a sieve and the arrival of prop- Abbreviations: ITS, internal transcribed spacer region of the nuclear rDNA; Mya, million years ago. Data deposition: The sequences reported in this paper have been The publication costs of this article were defrayed in part by page charge deposited in the GenBank data base (accession nos. L48115-L48176 payment. This article must therefore be hereby marked "advertisement" in and L48287-L48338). accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 7743 Downloaded by guest on September 27, 2021 7744 Evolution: Kim et al. Proc. Natl. Acad. Sci. USA 93 (1996)

a version 3.0 (35). Aligned sequences are available upon request Islands from the first author. Variable nucleotide sites were analyzed by unweighted Wagner parsimony using PAUP version 3.1.1 (36). On the basis of previous analyses of the Sonchinae (28), Islands was used as an outgroup. The heuristic algorithm with stepwise addition option was used to fiad the shortest trees. Bootstrap Selvagens Islands N, (100 replicates) and decay analyses were performed to assess the relative support for clades found in the analysis (37). Canary Islands,- Pairwise sequence divergences were calculated by the Jukes ,,- --- Tropic of Cancer and Cantor one-parameter method using PHYLIP version 3.52c (38). To assess rate homogeneity over different lineages, the relative-rate test (39, 40) was conducted using the Lactucosonchus as the reference taxon because this lineage is sister to the remainder of the alliance. Lslands RESULTS Size of ITS, Sequence Divergence, and Relative-Rate Test. Lengths of ITS1 and ITS2 in the woody Sonchus alliance fall b within the size range reported for Asteraceae (41). Percent pairwise sequence divergence between species ranges from 0.0 CANARY ISLANDS ' to 4.8, and average divergences within subg. Dendrosonchus LA(15.5) and Taeckholmia are 1.6% and 1.0%, respectively. Average sequence divergence between subg. Dendrosonchus (excluding TE( 11.6) Taeckholmia) and other genera in the alliance varies from 2.5% to 3.4%. PA(1.5) Results of the relative rate tests indicate no significant differences for any of the lineages, and thus the molecular FU(20.7) clock cannot be rejected. gS GO(12.5) Phylogenetic Analyses of ITS Sequences. After the previous GC(13.9) phylogenetic study of the Sonchinae, which suggests the mono- HI(>0.7) phyly of the woody Sonchus alliance in Macaronesia (Fig. 2), additional phylogenetic analyses of ITS sequences with a much 0 10OKm broader sampling within the group were carried out. The heuristic search option for 35 accessions found 8123 equally most trees, one in 3. This FIG. 1. (a) The dashed line encloses the biogeographical region of parsimonious of which is shown Fig. Macaronesia (17), which includes northwestern Africa and five archi- tree is identical to the 50% majority-rule consensus tree and pelagos. (b) The Canary archipelago and the oldest published radio- suggests that Sventenia, Babcockia, Prenanthes pendula, and metric ages from subaerial volcanics of each island in parenentheses Sonchus tuberifer are in turn sister groups to subg. Dendroson- (17-22). Abbreviations of islands are as follows: LA, Lanzarote [15.5 chus sensu Aldridge. It also suggests that Lactucosonchus, an million years ago (Mya)]; FU, Fuerteventura (20.7 Mya); GC, Gran endemic genus from the island of La Palma (Fig. lb), is sister Canaria (13.9 Mya); TE, Tenerife (11.6 Mya); GO, La Gomera (12.5 to the remaining members ofthe woody Sonchus alliance (Fig. 3). Mya); PA, La Palma (1.5 Mya); HI, Hierro (>0.7 Mya).

Hawaii contrasts with the situation in Macaronesia where a DISCUSSION source area is within 100 km of certain islands (Fig. 1). Origin and Evolution of the Woody Sonchus Alliance in In this study, sequences from the internal transcribed spacer Macaronesia. The molecular data strongly confirm and extend region of the nuclear ribosomal DNA (ITS) were used to assess considerably our previous preliminary work and indicate that, further the monophyly of the woody Sonchus alliance in the despite the extensive morphological and ecological diversity of Macaronesian islands. The sequence data were also used to the plants and the geographical proximity of the Macaronesian elucidate phylogenetic relationships within the group and the islands to a continental source area, the entire alliance was role of colonization and adaptive radiation in the evolution of derived from a single colonization event (Figs. 2 and 3). Both the alliance and to examine the origin of woody members of bootstrap and decay analyses support strongly the monophyly Sonchus in Macaronesia. of the group. The presence of intergeneric hybrids (32, 42) and results of crossing experiments (A. Aldridge, personal com- MATERIALS AND METHODS munication) likewise suggest genetic cohesiveness despite the considerable morphological diversity of the alliance. These A phylogenetic analysis of subtribe Sonchinae was conducted results are similar to those for other insular groups such as the previously, with limited sampling from the Macaronesian taxa genus Argyranthemum in the Macaronesian islands (43) and (ref. 28; Fig. 2). After this analysis, we examined the ITS the silversword alliance (10, 33) and Tetramolopium (44) in sequences of 35 additional accessions representing 16 species Hawaii, where highly fertile interspecific hybrids can be pro- of subg. Dendrosonchus, five species of Taeckholmia, and the duced despite pronounced morphological differences. Within four related genera endemic to the Canary Islands. Total DNA the woody Sonchus group, the ITS tree suggests that Lactu- was isolated from tissues by using the CTAB method (34) cosonchus diverged first, followed by the radiation of the four and purified in CsCl/ethidium bromide gradients. Methods for other genera, as well as subg. Dendrosonchus sensu Aldridge PCR amplification, purification of PCR products, and se- (Fig. 3). It is also likely that, based on the previous study of the quencing reactions of the ITS regions are given in detail Sonchinae (ref. 28; Fig. 2), the entire group was derived from elsewhere (11, 28). Both coding and noncoding strands were a single dispersal event from a more widely distributed Euro- read and all sequences were manually aligned using MACCLADE pean taxon, such as S. palustris. The low average sequence Downloaded by guest on September 27, 2021 Evolution: Kim et al. Proc. Natl. Acad. Sci. USA 93 (1996) 7745

Krigia montana Microseris laciniata Pyrrhopappus multicaulis Outgroups perenis Lactuca sativa Prenanthes purpurea - Prenanthes - Tarxacum Prenanthes altissima - Prenanthes Reichardia picroides - Reichardia tinginata Relchardla Reichardia ligulata _ arborescens _ Launaea nudicaulis j Launaea bulbosa -Aetheorhiza Sonchus kirkii Sonchus subg. Sonchus Sonchus bourgeaui Sventenia bupleuroides Babcockiaplatylepis Prenanthes pendula(N) Prenanthes pendula(S) Sonchus tuberifer Sonchus canariensis The woody Sonchus congestus Sonchus Sonchus fruticosus alliance In the Sonchus gonzalezpadroni Macaroneslan Sonchus ortunoi Islands Taeckholmia pinnata Taeckholmia canariensis Taeckholmia heterophylla Taeckholmia arborea Lactucosonchus webbli Sonchus palustris SSonchusaubg. Sonchus maritimus J Sonchus Kirkianella novae-zelandiae Kirkianella Embergeria grandifolia - Embergerla litoralis Dendroseris marginata Dendrosenis macrantha Dendrosefis micrantha r Dendroseris pruinata (TDendroerJuan Dendroseris neriifolia Fhe Dendrosenis pinnata Felande)Fernancdezhie Dendroseris berteroana Dendrosenis regia _ Sonchus luxurians U Sonchussubg. Sonchus schweinfurthii .. Sonchus

FIG. 2. ITS phylogeny of subtribe Sonchinae (redrawn from ref. 28). This is one of the 144 equally most parsimonious trees (consistency index = 0.526; retention index = 0.743). Dashed lines indicate branches that collapse in strict consensus tree. Numbers above in parentheses and below branches represent decay and percentage of bootstrap values, respectively. Arrow indicates the clade of woody Sonchus alliance. divergence and the polytomy in the ITS tree suggest a rapid land differentiation have played important roles in the evolu- radiation of major lineages early in the history of the alliance tion of the alliance (Fig. 3). Note, for example, that S. after a single introduction. canariensis occurs on two islands, as do S. hierrensis, S. acaulis, Adaptive radiation connotes the process by which a mono- S. cogestus, and T. pinnata as well as other species (Fig. 3). phyletic group of organisms adapts to a broad diversity of Further, long distance dispersal has been responsible for the habitats (3, 4), and it has been of major importance in the origin of Sonchus species in other archipelagos (Fig. 3). For evolution of woody Sonchus and its close relatives. The ITS example, S. daltonii in the Cape Verde archipelago likely phylogeny suggests that eight ecological shifts from mesic to results from a recent dispersal event from the western Canary dry habitats and three shifts from dry to coastal habitats have Islands. Also, three species of Sonchus in Madeira appear to occurred during the diversification of the group (Fig. 3). Two be derived from a single colonization event, probably from lineages of Taeckholmia (excluding two species of Sonchus) Tenerife or of the Canary Islands (Fig. 3). have radiated exclusively into dry habitats, whereas a major Biogeographical Implications. The molecular data suggest clade of Sonchus has radiated primarily into mesic habitats that, after the initial divergence of Lactucosonchus from a with two ecological shifts to dry habitats. The ITS phylogeny common ancestor, the two genera Sventenia and Babcockia as also indicates that, during adaptive radiation, rosette-shrub/ well as Prenanthespendula and S. tuberifer radiated early in the subshrub and rosette-tree habits have been quite successful in Canary Islands. These taxa are confined to mountains or colonizing and adapting to the various habitats of the islands. mountain cliffs ofthe geologically oldest areas of Gran Canaria In contrast, two lineages with tubers have only one species and Tenerife (with the exception of P. pendula, which is also each, i.e., S. tuberifer and Lactucosonchus, and have not been locally common in the south and west of Gran Canaria), and successful in radiating and speciating in the Macaronesian suggests that the woody Sonchus group arose in the Canary islands (Fig. 3). Islands. Further, it indicates that subg. Dendrosonchus and The ITS phylogeny also provides evidence that interisland Taeckholmia probably originated in the geologically oldest colonization events to similar ecological habitats and intrais- areas of Gran Canaria or Tenerife; remarkably these two Downloaded by guest on September 27, 2021 7746 Evolution: Kim et aL Proc. Natl. Acad. Sci. USA 93 (1996)

I Sventenia bupleuroides (GC; cp) D Babockia platylepis (GC; s) D 2 | Prenanthespendula (GC-N; s) 81% I_. Prenanthespendula (GC-S; s) Sonchus tuberifer (TE; hp) _ Sonchus subg. Sonchus D mq|- S. pinnatifidus (LA; t) - r S. brachylobus (GC; s) S. daltonii (CAPE VERDE; cp) S. hierrensis (GO; t) 15% S. hierrensis (PA; t) S. gandogeri (HI; t) S. palmensis (PA; t) Sonchus S. canariensis (TE; t) subg. S. canarensis (GC; t) Dendro- S. acaulis (GC; cp) sonchus S. acaulis (TE; cp) S. congestus (TE, GC; t) S. pinnatus (MADEIRA; t) M Sonchus S. fruticosus (MADEIRA; t) subg. S. ustulatus (MADEIRA; cp) Dendro- sonchus 100, S. fauces-orci (TE; cp) sensu S. gonzalezpadroni (GO; cp) Aldridge S. ortunoi (GO; cp) T. pinnata (GC,TE; s) )m T. pinnata var. microcarpa (TE; T. canariensis (GO; s) T. heterophylla (GO-1; s) Taeckholmia 2 T. capillaris (TE; a) 40%6 T. heterophylla (GO-2; a) T. arborea (TE; t) T. arborea (PA; t) J Iy: Lactucosonchus webbii (PA-1; hp) 94% Lactucosonchus webbii (PA-2; hp) Sonchus palustris (EUROPE; hp)

FIG. 3. Preferred ITS phylogeny of the woody Macaronesian Sonchus and their alliance. This is one of the 8123 equally most parsimonious trees (consistency index = 0.821; retention index = 0.821) and is identical to the 50% majority-rule consensus tree. Dashed lines and numbers above and below branches as in Fig. 2. Abbreviations of islands as in Fig. 1. Abbreviations of habits are as follows: hp, herbaceous perennial; cp, caudex perennial; s, rosette subshrub; t, rosette tree/shrub. Abbreviation of habitats are as follows: M, mesic; D, dry; C, coastal.

islands are also the center of diversity for subg. Dendrosonchus esian taxa is 3.34%, indicating that the divergence between and Taeckholmia (45). them may have occurred 4.2 million years ago (Mya). The Because the molecular clock cannot be rejected, it is possible average sequence divergence between subg. Dendrosonchus to estimate the time of the radiation of the woody Sonchus (including Taeckholmia) and allied genera is 2.8%. Thus, the alliance. The genus Dendroseris, which is endemic to the Juan divergence of subg. Dendrosonchus from the other genera may Fernandez Islands, was used to estimate the rate of nucleotide have occurred approximately 3.6 Mya. Therefore, the origin of substitution in ITS because both chloroplast (cp) DNA restric- genera in the woody Sonchus alliance may have taken place tion sites (46) and ITS sequence data (28) suggest that it is about 4.2 Mya or earlier on the Canary Islands, and the took be- closely related to the Macaronesian group. In addition, Den- radiation of subg. Dendrosonchus accordingly place tween 4.2 and 3.6 Mya on Gran Canaria or Tenerife. However, droseris is an insular endemic and has life forms similar to subg. if we use the faster rate, i.e., 1.20% per million years, then the Dendrosonchus (i.e., paliform and rosette trees to rosette origin of the alliance and the radiation of subg. Dendrosonchus shrubs). Thus, generation-time effect on the substitution rate may have occurred 2.8 Mya or earlier and 2.3 Mya, respec- of the ITS sequences should be minimized (16). Two different tively. Although all the colonization events of Sonchus species average rates of nucleotide substitutions per site per year in in the Macaronesian islands postdate the geological origin of ITS in the genus Dendroseris, r = (3.94 ± 0.10) x 10-9 and the islands (47), the calculated time of occurrence of Lactu- (6.06 ± 0.15) x 10-9, were used to estimate the time of cosonchus in La Palma predates the origin of the island (not radiation. The slower rate assumes radiation shortly after the older than 1.5 Mya; Fig. lb). This suggests that the immediate formation of the island of Masatierra (one of the Juan ancestor of Lactucosonchus evolved for some time on another Fernandez Islands), whereas the faster rate assumes a later island in the Canaries, either Tenerife or Gran Canaria, radiation and was estimated from cpDNA divergence. The followed by extinction of Lactucosonchus or its ancestor on slower rate for the sequences using Dendroseris as the standard such a source island. was 0.78% per million years (11). The average sequence The estimated divergence times for the allied genera and the divergence between Lactucosonchus and the other Macaron- radiation of subg. Dendrosonchus are long after the formation Downloaded by guest on September 27, 2021 Evolution: Kim et al. Proc. Natl. Acad. Sci. USA 93 (1996) 7747 of the Canary Islands, except the two westernmost ones, La plants (4). Thus, the molecular data do not support subg. Palma and El Hierro. Even assuming some uncertainty in Dendrosonchus being relictually woody plants. dating the ages of the older islands, it seems highly likely that In conclusion, the woody Sonchus alliance in the Macaro- their ages are still considerably older than the calculated time nesian islands apparently resulted from a single introduction. of radiation for Sonchus and its relatives. One question then is This founder event was likely followed by several radiations. why Sonchus was so successful if radiation occurred after the The ITS phylogeny refutes the relictural nature of the woody islands were several million years old and presumably open life form of Sonchus in Macaronesia and suggests that it habitats were not plentiful. One hypothesis is that extinctions represents secondary derivation from herbaceous ancestors. in the Canaries and northwestern Africa during the first The ITS sequence data also suggest that evolution ofthe woody glaciation in the Northern Hemisphere (2.8 Mya; ref. 48) and Sonchus alliance may have occurred during Late Tertiary (i.e., the beginning of Sahara desertification (2.5 Mya; ref. 49) may the late Miocene or early Pliocene) from Gran Canaria or have provided many open habitats for the radiation of the Tenerife in the Canary Islands. The rapid radiation of major alliance. The estimated divergence times, using the faster lineages in the alliance is consistent with an unresolved poly- mutations rate for Dendroseris in the calculations, coincide tomy at the base of the cladogram and low sequence divergence. closely with glaciation and desertification. The Origin of the Woody Sonchus in Macaronesia and We thank Aguedo Marrero, Pedro Ortega-Machin, and Francisco Insular Woodiness. The origin of woody Sonchus in Macaro- Jose Gonzalez Artiles for assistance during a field trip in the Canary nesia is controversial. Boulos (50) proposed that subg. Den- Islands. Also, Instituto Canario de Investigaciones Agrarias in Tener- (endemic to ife, through the advice of Manuel Fernandez-Galvan, provided finan- drosonchus evolved from subg. Origosonchus cial support for field studies to one of us (J.F.O.). We are indebted to Africa), which he considered the most primitive group of Charles Jeffrey and Kare Bremer for helpful suggestions about Sonchus. This hypothesis is supported by pollen morphology outgroups and are grateful to Robert Jansen, Eric Knox, Tom Myers, (51). In contrast, Aldridge (45) suggested that subg. Den- David Glenny, P.J. Garnock-Jones, Loutfy Boulos, and other people drosonchus is very primitive and that the two subgenera for providing plant and DNA materials. We thank Angela Aldridge for Origosonchus and Sonchus were derived from it. Her hypoth- her helpful discussion about this project. We are especially indebted esis is congruent with Takhtajan's view (52) and also agrees to Sherwin Carlquist for many helpful comments and suggestions on with Bramwell (24, 25). Neither of these two hypotheses is an earlier version of this paper. This work was supported by Sigma Xi supported by the ITS phylogeny. The ITS phylogeny indicates Grants-in-Aid of Research, Graduate Student Research Grant from American Society of Plant Taxonomists, Tinker Foundation (Latin that subg. Dendrosonchus is a relatively derived group but was American Studies Program, Ohio State University), Janice Beatley not derived directly from subg. Origosonchus (Figs. 2 and 3). Herbarium Award (Ohio State University Herbarium) to S.-C.K., and Rather, it is more likely that it originated from an ancestor National Science Foundation Doctoral Dissertation Improvement somewhat like one of its allied genera in the Canary Islands Grant DEB-9521017 to D.J.C. and S.-C.K. (Fig. 3). The woody life-forms in the Canaries in genera such as 1. Carlquist, S. (1965) Island Life (The Natural History Press, New Sonchus, Echium,Argyranthemum, Pericallis, and Crambe have York). been considered by several authors to represent tertiary relicts 2. Carlquist, S. (1970) Hawaii: A Natural History (The Natural (6, 17, 24, 53-55). Bramwell (24) suggested that taxonomic, History Press, New York). morphological, palaeobotanical, distributional, 3. Carlquist, S. (1974) Island Biology (Columbia Univ. Press, New cytological, York). and phytogeographical data are consistent with the endemic 4. Carlquist, S. (1995) in Hawaiian Biogeography: Evolution on a Hot flora being of considerable age and probably ancestral to many SpotArchipelago, eds. Wagner, W. & Funk V. (Smithsonian Inst., modern Mediterranean genera and species. Meusel (53) Washington, DC), pp. 1-13. viewed the woody Macaronesian species as ancestral forms of 5. Lack, D. (1947) Da,win's Finches (Cambridge Univ. Press, New modern Mediterranean herbaceous species, with the herba- York). ceous forms derived by reduction in lignification and adapta- 6. Bramwell. D. (1975) Anal. Inst. Bot. Cavanilles 32, 241-254. tion to more extreme conditions. In contrast, Carlquist (2-4) 7. Baldwin, B. G., Kyhos, D. W. & Dvorak, J. (1990) Ann. Mo. Bot. argued that the endemic frutescent species found on many Gard. 77, 96-109. oceanic islands are the result of an increase in woodiness in 8. Carr, G. D. & Kyhos, D. W. (1981) Evolution 35, 543-556. 9. Helenurm, K. & Ganders, F. (1985) Evolution 39, 753-765. response to the uniformity of insular . More specifi- 10. Baldwin, B. G., Kyhos, D. W., Dvorak, J. & Carr, G. D. (1991) cally, Carlquist (3) claimed that a group of true shrubby Proc. Natl. Acad. Sci. USA 88, 1840-1843. Sonchus in the Macaronesian Islands evolved from plants 11. Sang, T., Crawford, D. J., Kim, S.-C. & Stuessy, T. F. (1994) similar to the European weedy sow (S. oleraceus). Thus, Am. J. Bot. 81, 1494-1501. he did not consider these plants to be relicts but rather 12. Sanders, R. W., Stuessy, T. F., Marticorena, C. & Silva, 0. M. secondary derivatives of herbaceous ancestors. The ITS tree (1987) Opera Bot. 92, 195-215. clearly shows that neither subg. Sonchus nor subg. Origoson- 13. Givnish, T. J., Sytsma, K. J., Smith, J. F. & Hahn, W. J. (1994) chus was derived from the woody members of Sonchus in Proc. Natl. Acad. Sci. USA 91, 2810-2814. Macaronesia it is evident that the woody 14. Sang, T., Crawford, D. J., Stuessy, T. F. & Silva, 0. M. (1995) (Fig. 2). Rather, Syst. Bot. 20, 55-64. Sonchus and its relatives were derived ultimately from conti- 15. Baldwin, B. G. (1992) Mol. Phylogenet. Evol. 1, 3-16. nental herbaceous perennial ancestors (Fig. 3). Further, the 16. Soltis, P. S. & Soltis, D. E. (1995) in Evolutionary Biology, eds. ITS tree shows a general trend toward increased woodiness. Hecht, M. K., Macintyre, R. J. & Clegg, M. T. (Plenum, New For example, it is likely that the ancestor of the entire alliance York), pp. 139-194. was an herbaceous perennial, and then there was evolution 17. Sunding, P. (1979) in Plants and Islands, ed. Bramwell, D. toward caudex perennials, shrubs, and trees in different lin- (Academic, New York), pp. 13-40. eages during radiation in the Macaronesian islands (Fig. 3). In 18. McDougall, I. & Schmincke, H. U. (1976-1977) Bull. Volcanol. particular, it seems reasonable to assume that the immediate 40, 57-77. and the 19. Banda, E., Danobeitia, J. J., Surinach, E. & Ansorge, J. 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