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Hybridization in the Evolution of the Macaronesian Flora Proc. Natl. Acad. Sci. USA Vol. 93, pp. 4085-4090, April 1996 Evolution Chloroplast DNA evidence of colonization, adaptive radiation, and hybridization in the evolution of the Macaronesian flora (oceanic island flora/Atlantic islands/biogeography/Angiosperms/Argyranthemum) JAVIER FRANCISCO-ORTEGA*, ROBERT K. JANSEN*t, AND ARNOLDO SANTOS-GUERRA: *Department of Botany, University of Texas, Austin, TX 78713-7640; and tJardin de Aclimataci6n de La Orotava, Puerto de La Cruz, Tenerife 38400, Canary Islands, Spain Communicated by Thomas N. Taylor, University ofKansas, Lawrence, KS, December 14, 1995 (received for review June 16, 1995) ABSTRACT Most evolutionary studies of oceanic islands cene, when the first northern hemisphere glaciation and the have focused on the Pacific Ocean. There are very few exam- desertification of most of northern Africa led to massive ples from the Atlantic archipelagos, especially Macaronesia, extinction and migration of plants and animals (15). despite their unusual combination of features, including a Macaronesia, like other tropical and subtropical volcanic close proximity to the continent, a broad range of geological archipelagos, is under the influence of the trade winds. These ages, and a biota linked to a source area that existed in the winds, in combination with altitudinal gradients on the islands, Mediterranean basin before the late Tertiary. A chloroplast have produced several distinct ecological zones (15). Two main DNA (cpDNA) restriction site analysis of Argyranthemum climatic regions can be distinguished. The first is under the (Asteraceae: Anthemideae), the largest endemic genus of influence of humid and cool northeastern trade winds and plants of any volcanic archipelago in the Atlantic Ocean, was mainly covers a band in the north of the islands between 400 performed to examine patterns of plant evolution in Maca- and 1200 m. This region has three main ecological zones: ronesia. cpDNA data indicated that Argyranthemum is a humid lowland scrub, laurel forest, and heath belt (Table 1). monophyletic group that has speciated recently. The cpDNA In contrast, the second climatic region is not under the tree showed a weak correlation with the current sectional influence of the trade winds and is more arid. This area is classification and insular distribution. Two major cpDNA restricted to the southern slopes of the islands, in the north at lineages were identified. One was restricted to northern altitudes higher than 1200 m and in the coastal belt below 400 archipelagos-e.g., Madeira, Desertas, and Selvagens-and m. Four major ecological zones are recognized in the arid the second comprised taxa endemic to the southern archipel- climatic region: coastal desert, arid lowland scrub, Canarypine ago-e.g., the Canary Islands. The two major radiations forest, and high altitude desert (Table 1). In many instances, identified in the Canaries are correlated with distinct ecolog- the northeastern trade winds can also have an influence on the ical habitats; one is restricted to ecological zones under the southern slopes of some of the islands (18). This is especially influence of the northeastern trade winds and the other to true in the islands where the summit barely reaches 1200 m. In regions that are not affected by these winds. The patterns of these cases, the laurel forest can also spread toward the phylogenetic relationships in Argyranthemum indicate that southern slopes and a humid lowland scrub is found below that interisland colonization between similar ecological zones is forest in the south or west. the main mechanism for establishing founder populations. The high diversity of habitats appears to be one of the main This phenomenon, combined with rapid radiation into distinct factors responsible for the rich Macaronesian flora, which ecological zones and interspecific hybridization, is the pri- includes -700 endemic species (19). The largest endemic plant mary explanation for species diversification. genus (Argyranthemum) of all Atlantic Ocean volcanic islands occurs in these archipelagos (20, 21). Its 23 species provide the Oceanic islands provide model systems to assess organismic most spectacular example of speciation in Macaronesia (22), evolution following colonization and isolation. Classical stud- and at least one species is endemic to each of the major ies of the Galapagos finches (1) and Hawaiian Drosophila (2) ecological zones (Table 1). Thus, Argyranthemum is an ideal have had a major impact on the history of evolutionary thought group to examine patterns of speciation in Macaronesia. in the 19th and 20th centuries. Oceanic islands are relatively Further justification for studying this genus is that the closest simple systems where both patterns of dispersal and natural relatives (Chrysanthemum and Heteranthemis) have been selection can be more easily assessed than in continental identified from the continent (refs. 23-27; J.F.-O., R.K.J., systems. Most studies ofisland biota have been restricted to the A. Hines, and A.S.-G., unpublished data). Pacific Ocean archipelagos of Hawaii (3-6), Galapagos (7, 8), We used Argyranthemum as an example to assess the origin and Juan Fernandez (9-11). Few studies (12, 13) have focused and evolution of the Macaronesian flora. Phylogenies gener- on the Atlantic Ocean archipelagos that constitute the bio- ated from chloroplast DNA (cpDNA) data were used to geographical region known as Macaronesia (Fig. 1). These examine the role of colonization, adaptive radiation, and archipelagos have several unique features that make them hybridization in the evolution of endemic plants from the ideal systems for understanding the origin and evolution of Atlantic archipelagos. The approach is similar to previous island floras and faunas. Macaronesia comprises five major studies of endemic genera from three volcanic archipelagos archipelagos (Azores, Canaries, Cape Verde, Madeira, and from the Pacific Ocean: Dendroseris (9) and Robinsonia (10) in Selvagens) that exhibit a broad range of geological ages from the Juan Fernandez Islands; the silversword alliance (3) and 0.8 to 21 million years (14). The region is in close proximity to Cyanea (6) in the Hawaiian Islands; and Gossypium in the the continent, unlike most volcanic archipelagos. In addition, Galapagos (8) and Hawaiian (28) Islands. In all of these cases, the Macaronesian biota has been linked to one that spread cpDNA restriction site analyses were informative and provided from the Mediterranean basin in the late Miocene and Plio- evidence for rapid speciation, hybridization, and colonization in the flora of Pacific archipelagos. The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in Abbreviation: cpDNA, chloroplast DNA. accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 4085 Downloaded by guest on September 29, 2021 4086 Evolution: Francisco-Ortega et al. Proc. Natl. Acad. Sci. USA 93 (1996) weights from 1.01:1 to 2.5:1 of site gains/losses with ancestral states designated as Os (35). Bootstrap values (36) from 100 replicates were calculated to assess the amount of support for monophyletic groups. Maximum likelihood values were esti- mated for a subset of trees in the 15-taxon analysis using the RESTML program of PHYLIP (37). Estimates of nucleotide sequence divergence were also computed using equations 9 and 10 of Nei and Li (38). Values were calculated only for the 6-bp enzymes because of the availability of complete restriction maps. Sequence divergence was calculated among 11 taxa, including the four outgroups and seven Argyranthemum species from the three major lin- eages identified in the phylogenetic analyses of the complete data set. RESULTS The 21 restriction enzymes identified '3190 restriction sites (978 from 6-bp enzymes and 2112 from 4-bp enzymes) in cpDNAs of each species. This represents 14,716 bp, or 11% of the chloroplast genome of each taxon. A total of 151 variable restriction sites was detected, 84 of which were phylogeneti- cally informative. Wagner parsimony yielded 54 equally par- simonious trees of 172 steps with a consistency index of 0.80 (excluding uninformative changes) and a retention index of 0.967. The trees provided strong support (14 characters, 100% bootstrap value) for the monophyly of Argyranthemum. Two FIG. 1. The Macaronesian islands (inset) and the distribution of major clades were resolved in the genus (Fig. 2A). One clade Argyranthemum in the Madeira, Selvagen, and Canary archipelagos. included taxa endemic to the Canaries (Canarian clade), Blackened islands are those where Argyranthemum occurs. whereas the second one comprised only species from Madeira, Selvagens, and Desertas (Madeiran clade). The Canarian clade Our investigation identified a strong and unexpected cor- consisted of two clades (A and B), which collapsed in the strict relation between the two major climatic regions of Macaro- consensus tree (Fig. 2A, dashed line). These three lineages nesia and the groups in the cpDNA phylogeny. Patterns of (one Madeiran and two Canarian) were detected in all 54 phylogenetic relationships in Argyranthemum indicate that equally parsimonious trees and their relationships were re- interisland colonization between similar ecological zones, solved in three different ways: (i) Madeira sister to the Canary adaptive radiation, and hybridization have all played an im- Islands, (ii) one of the two canary clades sister to
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