In the Macaronesian Islands: Molecular Evidence for Extensive Radiation (Adaptive Radiation/Molecular Evolution/Biogeography) SEUNG-CHUL KIM*, DANIEL J
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Proc. Natl. Acad. Sci. USA Vol. 93, pp. 7743-7748, July 1996 Evolution A common origin for woody Sonchus 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 Plant 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, Tenerife, Canary Islands, Spain 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 plants 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 Mediterranean basin 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 (Asteraceae) 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 habitats. 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 Prenanthes. 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 roots. 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 Azores Islands from the first author. Europe 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), Sonchus palustris Madeira Islands was used as an outgroup. The heuristic algorithm with stepwise addition option was used to fiad the shortest trees. Bootstrap Selvagens Islands N, Africa (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 genus Lactucosonchus as the reference taxon because this lineage is sister to the remainder of the alliance. Cape Verde 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.