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Systematics |
2Department of Biological Sciences, Florida International University, and Fairchild Tropical Garden, Miami, Florida 33199 USA; 3Real Jardín Botánico, Madrid, 28014 Spain; 4Department of Botany and Plant Science, University of California, Riverside, California 92521 USA; 5Jardín de Aclimatación de La Orotava, Tenerife, 38400 Spain; 6Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045 USA; 7Section of Integrative Biology, University of Texas, Austin, Texas 78712 USA
Received for publication January 3, 2002. Accepted for publication June 27, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: adaptive radiation • angiosperms • biodiversity • biogeography • Crambe • evolution • Macaronesia • molecular systematics • oceanic islands • speciation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). A phylogenetic analysis of the internal transcribed spacer (ITS) regions of nuclear ribosomal DNA (rDNA) showed that Crambe comprises three major monophyletic groups (Francisco-Ortega et al., 1999
). One of these groups, Crambe sect. Dendrocrambe DC., has 14 species (Santos-Guerra, 1996
; Prina, 2000
) and is endemic to the Macaronesian archipelagos of the Canary Islands (13 species) and Madeira (1 species). Each of the Canary Islands has at least one endemic species from this section, with the exception of Lanzarote where no species of Crambe occur (Fig. 1). The only Madeiran species, C. fruticosa, also occurs on the islands of Desertas and Porto Santo. Another species that occurs on more than one island is C. strigosa, an endemic of Tenerife and La Gomera. Reports of C. santosii on La Gomera and Tenerife and of C. strigosa on La Palma (Carqué-Alamo et al., 1997
; Prina, 2000
) need further investigation.
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; Fig. 1). This vegetation zone is found on northern slopes of the islands, which are under the direct influence of the humid and cool northeastern trade winds, and receive up to 1000 mm of rainfall per year (Fernández-Palacios, 1999
). Traditionally, the laurel forest in Macaronesia has been considered a relict of an ecological zone that existed in the Mediterranean basin during the Miocene (Quézel, 1995
; Nakamura et al., 2000
). Fossil data from southern Europe support this hypothesis (reviewed by Sunding, 1979
). However, recent phylogenetic studies indicate that some endemics in the laurel forest have a post-Tertiary origin and cannot be considered directly linked to the Miocene vegetation of southern Europe (Carvalho and Culham, 1998
; Thiv, Struwe, and Kadereit, 1999
). A post-Tertiary origin for species of the laurel forest has been reported primarily for plants in the understory; few studies have included canopy trees and most of the canopy species do not show major radiations in Macaronesia.
Nine species of Crambe sect. Dendrocrambe are restricted to the lowland scrub (Oleo-Rhamnetalia crenulatae) (Fig. 1). This vegetation zone is situated above the coastal xerophytic belt (Kleinio-Euphorbietalia canariensis) and receives up to 550 mm of rainfall per year (Fernández-Palacios, 1999
). The two species in the pine forest (Chamaecytiso-Pinetalia canariensis) are also found in other ecological zones. This type of pine forest is restricted to the Canary Islands and is situated above the laurel forest (on northern slopes of the islands) or above the lowland scrub (on southern slopes). The only islands without pine forest are Fuerteventura and Lanzarote. Rainfall in this forest ranges between 400 and 800 mm per year.
The recently described C. tamadababensis from Gran Canaria is found both in the pine forest and in the lowland scrub (Prina and Marrero-Rodríguez, 2000
). Likewise C. microcarpa from La Palma can be found in both the pine forest and the laurel forest zones of this island. Endemic species of Crambe do not occur in the coastal xerophytic belt or in the high altitude scrub (Spartocytision supranubii). The direction of evolutionary change in habitat preference in sect. Dendrocrambe is ambiguous because species are present in three of the major ecological zones of Macaronesia.
In this paper, we present a phylogenetic study of the species of sect. Dendrocrambe based on nucleotide sequences of the ITS regions of nuclear rDNA. Previous studies have shown that in many cases the ITS can provide enough phylogenetic signal to estimate phylogenies of island groups (Baldwin et al., 1998
). The main objectives of this research were to clarify the phylogenetic relationships of the Macaronesian species of Crambe and to use the molecular phylogeny to understand the biogeographical, ecological, and morphological patterns of variation in this group.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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).
DNA isolation, polymerase chain reaction (PCR) amplification, and direct sequencing of the ITS region for most species followed protocols used in Francisco-Ortega et al. (1999)
. Sequences of C. tamadababensis and C. wildpretii were obtained following the protocols of Fuertes-Aguilar, Rossello, and Nieto-Feliner (1999)
. Accession data are given in http://ajbsupp.botany.org/v89/.
Phylogenetic analyses
Sequences were easily aligned manually. All phylogenetic analyses were performed using version 4.0b5 of PAUP* (Swofford, 1999
). Maximum parsimony (MP) and maximum likelihood (ML) methods were used to reconstruct phylogenies. Due to computer memory limitations, the ML analyses only included one sequence from each of the ingroup species (the reduced data set of 17 species included in this analysis are marked with an asterisk in the table found at http://ajbsupp.botany.org/v89/). In contrast, maximum parsimony analyses included sequences from all 37 samples, although the reduced data set of the 17 species was used for parsimony optimization of biogeographical ecological features (see below).
In maximum parsimony analyses, nucleotide changes were weighted. Transversions were weighted over transitions by a 2 : 1 ratio based on the ML analysis (see below). Heuristic searches for most parsimonious trees were performed with 100 random entries using the ACCTRAN, MULTREES, and TBR options. Informative gaps were coded as binary characters (present or absent) and added to the original data matrix using the "simple indel coding" method for recoding of gaps (Simmons and Ochoterena, 2000
). The consistency index (CI; Kluge and Farris, 1969
) and the retention index (RI; Farris, 1989
) were also calculated. One hundred bootstrap replicates (Felsenstein, 1985
) were performed using a heuristic search with one random taxon entry.
The HKY85 model of DNA sequence evolution (Hasegawa, Kishino, and Yano, 1985
) with among-site variation approximating a gamma distribution was used in the ML analyses, and gaps were treated as missing data. The ML search involved estimation of parameters (i.e., transition/transversion ratios, proportion of invariant sites, base frequencies, and shape of the gamma distribution). Support for monophyletic groups was evaluated with 500 bootstrap replicates (Felsenstein, 1985
) using a heuristic search with ten random entries. Parameter values obtained from the initial ML search (see above) were used for the bootstrap analysis. Due to memory limitations, the number of trees saved in each bootstrap replicate was limited to a maximum of 500.
Character optimizations were performed using parsimony for three sets of characters using MacClade (Maddison and Maddison, 2000
): (1) ecology (with three states, laurel forest, lowland scrub, and pine forest); (2) insular distribution (with seven states, Fuerteventura, La Gomera, Gran Canaria, El Hierro, Madeira/Porto Santo, La Palma, and Tenerife); and (3) archipelago distribution (with two states, Canaries and Madeira). Character optimizations were mapped onto the two most parsimonious trees obtained after weighted parsimony analysis with the reduced data set of 17 species. Character states for ecological and island data of the outgroup taxa were coded as "0," and they were different from the states assigned to the island endemics.
Nucleotide sequence divergence values based on the HKY85 model of DNA sequence evolution were also estimated. A pairwise distance matrix was computed using the parameters estimated from the ML analysis (see below).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The two sequences of C. arborea are identical as are the three sequences of C. feuilleii. Other sets of identical sequences include two sequences of C. microcarpa (MICRO1 and MICRO2), four sequences of C. scaberrima (SCAB1, SCAB2, SCAB4, and SCAB5), and four sequences of C. strigosa-C. wildpretii (STRIG2, STRIG4, STRIG5, WILDP1). The two most divergent sequences of insular taxa are between the Madeiran species C. fruticosa (FRUTI3) and the Gran Canarian endemic C. scoparia (6.50% nucleotide sequence divergence).
Phylogenetic analyses
There are 91 variable sites, with 53% (48) of these being parsimony informative. Weighted parsimony analysis (transversions were weighted over transitions by a 2 : 1 ratio) yields six trees with 112 steps, a CI of 0.835 (excluding autapomorphies), and an RI of 0.940. One of the six most parsimonious trees and the strict consensus tree from this analysis are shown in Fig. 2. Weighted parsimony analyses with transversions weighted over transitions with weights of 1.1, 1.5, 2.1, and 2.5 also yield the same six tree topologies.
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The ML analysis of 17 species yields one tree (–ln = 1217.51871). Estimated base frequencies are A = 0.2427, C = 0.2511, G = 0.2456, T = 0.2606. Other estimated parameters are: transition/transversion ratio = 2.0 (kappa = 4.1110); proportion of invariable sites = 0.1326; and value of gamma shape parameter = 0.649206. The ML tree is identical to one of the two trees generated by weighted parsimony analyses of 17 species (Fig. 3). The ML tree agrees with the weighted parsimony tree in placing the two taxa of lineage 1 (from Madeira and Fuerteventura) sister to the rest of the insular species. Bootstrap support for this relationship is weak in both the ML (64%) and the weighted parsimony analysis (68%).
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). We show character optimizations for only one of the most parsimonious trees (Figs. 4–5). The other most parsimonious tree showed identical optimization results for these ecological and biogeographic data. The most parsimonious character optimizations for archipelago distribution, island distribution, and ecology require two, ten, and four steps, respectively (Figs. 4–5). The character reconstructions suggest that ancestral lineages of Crambe originated in the lowland scrub of the Canary Islands, followed by colonization of the laurel forest and pine forests of both the Canary and Madeira archipelagos. Tenerife is the most likely ancestral area of the lineages 2 and 3, and the Canary Islands probably represent the ancestral archipelago.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Santos-Guerra, 1990
; Thiv, Struwe, and Kadereit, 1999
). Many phytogeographers consider most laurel forest endemics to be relicts of a flora that was prevalent in the Mediterranean in the Pliocene and early Pleistocene. The ITS phylogeny of Crambe provides two insights into the origin of laurel forest species: (1) there have been two independent colonization events into this forest; and (2) patterns of ecological diversification are from lower elevation zones (lowland scrub) to higher elevations zones (laurel forest and pine forest).
Multiple colonizations of the laurel forest by congeneric species have been reported from the Aeonium Webb & Berthel. alliance (Crassulaceae) (Mort et al., 2002
), Hedera L. (Araliaceae) (Vargas et al., 1999
), Pericallis D. Don (Asteraceae) (Panero et al., 1999
), Sideritis L. (Lamiaceae) (Barber et al., 2000
), and Tolpis Adans. (Asteraceae) (Moore et al., 2002
). In most of these examples, taxa from the laurel forest are in a derived position, which suggests a relatively recent origin. The ITS tree for Crambe also indicates a recent colonization of the laurel forest. The most obvious case of recent colonization involves C. feuillei, an endemic from El Hierro in lineage 2 (Fig. 3). El Hierro is the youngest island of the Canary archipelago. The oldest subaerial rocks of this island are 1.12 million years old (Guillou et al., 1996
), indicating a post-Tertiary origin for species of Crambe endemic to the laurel forest of this island. The two other species of Crambe restricted to the laurel forest (C. santosii and C. strigosa, both in lineage 3) also appear to be derived based on the ITS data (Figs. 2–3).
Biogeographic relationships
The ITS phylogeny supports a floristic connection between the eastern Canary Island of Fuerteventura and the Madeiran archipelago. A multivariate analysis of the Macaronesian flora suggests that the Canarian and Madeira archipelagos form a distinct cluster (Nicolas et al., 1989
; La-Roche and Rodríguez-Piñero, 1994
). Previous phylogenetic studies of several plant genera suggest that the floras of the Canary Islands and Madeira are linked through the five western Canary Islands of El Hierro, Gran Canaria, La Gomera, La Palma, and Tenerife (e.g., Panero et al., 1999
; Mort et al., 2002
). The sister relationship between C. sventenii from Fuerteventura and C. fruticosa from Madeira provides the first phylogenetic evidence of a biogeographic connection between the eastern Canary Islands and Madeira. The two genera Crepis and Helichrysum in the Asteraceae may provide additional evidence of a connection between Madeira and the eastern Canary Islands because they are restricted primarily to these islands (Hansen and Sunding, 1993
; García-Casanova, Scholz, and Hernández, 1995
).
The ITS tree supports Tenerife as the ancestral island for the common ancestor of all the species in the five westernmost islands of Gran Canaria, Tenerife, La Gomera, La Palma, and El Hierro. Tenerife is the largest and most ecologically diverse of the Macaronesian Islands. This island is approximately 12 million year old (Ancochea et al., 1990
), and it is situated between the islands of Gran Canaria and Fuerteventura and the islands of La Gomera, El Hierro, and La Palma (Fig. 1). Previous phylogenetic studies of Macaronesian plants have not focused on identifying ancestral areas of dispersal. However, the age, large size, central location, and extraordinary ecological diversity of Tenerife suggest that this island may have played an important role as a center of dispersal in the Canary Islands.
Optimization of archipelago distribution on the ITS tree supports the Canary Islands as the ancestral archipelago. Thus, colonization in Crambe apparently occurred from the Canary Islands to Madeira. Phylogenetic evidence for the Sonchus L. alliance (Asteraceae) (Kim et al., 1996
) and Pericallis (Panero et al., 1999
) also support a dispersal route from the Canaries to Madeira.
The ITS phylogeny, unfortunately, does not resolve the issue of the direction of colonization between the eastern and the western Canaries and whether the island of Tenerife or Fuerteventura can be regarded as the ancestral island for the Macaronesian species of Crambe.
Taxonomy and morphology
A number of previous workers have discussed the morphology of this genus (Sventenius, 1953
; Bramwell, 1969a
, b
, 1973
; Prina, 2000
). The ITS phylogeny has some implications for the taxonomy of the Macaronesian species and for our understanding of patterns of morphological variation.
Crambe scoparia is one of the most morphologically distinctive species of sect. Dendrocrambe. It is the only species that sheds its leaves in summer and has fruits with a relatively long distal beak. The leaves also have a unique combination of features, including a glabrous and chartaceous texture, a reddish color, and few lobes. Sventenius (1953)
used these features to support the recognition of the distinct sect. Rhipocrambe. The ITS phylogeny does not support the segregation of C. scoparia at the sectional level because this species is nested within lineage 3 (Fig. 2).
There is a good correspondence between the monophyletic groups in the ITS tree and morphology. The Madeiran and Fuerteventuran species of lineage 1 share a combination of unique morphological features, including laterally compressed fruits and small, glabrous, and glaucous leaves with sinuate margins. These two species differ primarily in their fruit morphology with those of C. sventenii having two lateral wings, whereas the wings are either missing or greatly reduced in C. fruticosa.
Morphological similarities among species are also apparent in lineages 2 and 3. With the exception of C. wildpretii (Prina and Bramwell, 2000
), all five species in the largest clade of lineage 3 share several morphological features, including large, wide, pubescent leaves and lax, highly branched inflorescences with long peduncles. The five species of lineage 2 are similar in having small, rhomboid leaves with a hard texture and compact inflorescences with short peduncles.
The strong concordance between patterns of morphological variation and the groups present in the ITS tree of Crambe is rarely seen in other Macaronesian groups. Previous molecular phylogenies of Argyranthemum Sch. Bip. (Asteraceae) (Francisco-Ortega, Jansen, and Santos-Guerra, 1996
), the Aeonium alliance (Mort et al., 2002
), the Gonospermum Less. alliance (Asteraceae) (Francisco-Ortega et al., 2001
), Pericallis (Panero et al., 1999
), and Sideritis (Barber et al., 2000
) demonstrated that most of the morphologically defined sections in these genera are either paraphyletic or polyphyletic. The most extraordinary example of incongruence between morphology and molecular phylogenies is in Pericallis. It has been claimed that woodiness in this genus is a pleisomorphic character state (Nordenstam, 1978
; Serrada et al., 1988
). A recent molecular study indicates that woodiness is derived and that it originated multiple times (Panero et al., 1999
).
Conclusions
Our ITS phylogeny demonstrates that the Macaronesian species of Crambe have experienced multiple inter-island colonization events and that radiation of this group has involved several ecological shifts. Similar ecogeographic patterns have been detected for the majority of the endemics of these islands (i.e., the Aeonium alliance [Mort et al., 2002
], Sideritis [Barber et al., 2000
], and the Sonchus alliance [Kim et al., 1996
]), although in some cases, inter-island colonization among similar ecological zones has also been important (i.e., Argyranthemum; Francisco-Ortega, Jansen, and Santos-Guerra, 1996
; Francisco-Ortega et al., 2001
). Thus, Crambe follows the same phytogeographic patterns detected in many other Macaronesian endemics.
Crambe differs from other Macaronesian taxa because of the agreement between morphologically defined groups and the molecular phylogeny. Our results seem to indicate that hybridization has not played a major role in the evolutionary history of the Macaronesian species of Crambe. The common occurrence of natural hybrids in Argyranthemum and Sideritis has been used as an argument to explain the poor correlation between molecular phylogenies and the morphological groupings in these two genera (Francisco-Ortega et al., 1996
; Barber et al., 2000
; Brochmann, Borgen, and Stabbetorp, 2000
).
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FOOTNOTES |
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8 Author for reprint requests (ortegaj{at}fiu.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Ancochea E. J. M. Fúster E. Ibarrola A. Cendrero J. Coello F. Hernán J. M. Cantagrel C. Jamond 1990 Volcanic evolution of the island of Tenerife (Canary Islands) in the light of new K-Ar data. Journal of Volcanology and Geothermal Research 4: 141-155
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