| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Systematics |
2Section of Integrative Biology and Institute of Cellular and Molecular Biology, University of Texas, Austin, Texas 78712 USA; 3Department of Biological Sciences, Florida International University, University Park, Miami, Florida 33199 USA, and The Research Center, The Fairchild Tropical Garden, 11935 Old Cutler Road, Miami, Florida 33156 USA; 4Jardín de Aclimatación de La Orotava, Calle Retama Número 2, Puerto de la Cruz, Tenerife, Canary Islands E-38400 Spain
Received for publication March 15, 2001. Accepted for publication July 20, 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
13 species native to Africa, Europe, and Macaronesia, with at least one species endemic to each of the four major archipelagos of the Azores, Madeira Islands, Canary Islands, and Cape Verde Islands. All but two of these species develop woody stems by maturity. Chloroplast DNA restriction site variation was analyzed for all species of Tolpis and four outgroups in order to understand the patterns of island colonization and evolution of woodiness in this genus. Parsimony analyses revealed a strongly supported monophyletic Tolpis. Within the genus, the following three well-supported groups were detected: all species from the Canary Islands and Cape Verde Islands, both Azorean species, and both continental species. The Canary Island/Cape Verde clade was sister to the two continental species, and the Azorean clade was sister to this group. The two Madeiran species of Tolpis occupied the basalmost positions within the genus. When biogeography was mapped onto this phylogeny, nine equally parsimonious reconstructions (five steps each) of dispersal history were detected, which fell into two groups: eight reconstructions implied that Tolpis colonized Madeira from the continent, followed by continental extinction and subsequent continental recolonization, while one reconstruction implied that Tolpis colonized Macaronesia four times. Two of the reconstructions involving continental extinction required the least amount of overall dispersal distance. The cpDNA phylogeny also suggests that woodiness arose in the common ancestor of all extant Tolpis, followed by two independent reversals to an herbaceous habit. Assuming that one of the eight reconstructions favoring continental extinction and recolonization is true, our results suggest that Tolpis may represent the first documented example of a woody plant group in Macaronesia that has recolonized the mainland in herbaceous form.
Key Words: Asteraceae; chloroplast DNA phylogeny • Lactuceae • long-distance dispersal • Macaronesia • restriction site variation • Tolpis • woodiness
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Some examples of island plant groups that have recently been shown to result from a single dispersal event include the silversword alliance and the lobeliods in Hawaii (Baldwin and Robichaux, 1995
; Givnish et al., 1996
), Dendroseris D. Don in the Juan Fernández Islands (Kim, Crawford, and Jansen, 1996
), and Argyranthemum Sch.Bip. (Francisco-Ortega et al., 1997
) and the Sonchus L. alliance (Kim et al., 1996
) in Macaronesia. However, several instances of multiple colonizations of the same archipelago(s) have been documented recently as well: Rubus L. in Hawaii (Howarth, Gardner, and Morden, 1997
), Gossypium L. in the Galápagos Islands (Wendel and Percival, 1990
; Wendel, Schnabel, and Seelanan, 1995
), and Hedera L. (Vargas et al., 1999
), Ilex L. (Cuénoud et al., 2000
), Lavatera L. (Ray, 1995
; Fuertes-Aguilar et al., in press), and Olea L. (Hess, Kadereit, and Vargas, 2000
) in Macaronesia.
Tolpis Adanson (Asteraceae: Lactuceae) consists of 13 species that grow in the Mediterranean regions of Africa, Asia, and Europe and in all of the major archipelagos of Macaronesia (the Azores, Madeira Islands, Canary Islands, and Cape Verde Islands; Jarvis, 1980
). This genus is remarkable biogeographically because most of these species (11) are Macaronesian endemics, with at least one species native to each of the four major island groups (Fig. 1; Jarvis, 1980
). Only four other genera (Carex L. [Cyperaceae], Euphorbia L. [Euphorbiaceae], Festuca L. [Poaceae], and Lotus L. [Fabaceae]) have endemic species in each of these same archipelagos (Hansen and Sunding, 1993
). However, all of these genera are much more widespread outside of Macaronesia, both in number and geographic range of species, than Tolpis. The biogeography of Tolpis thus provides an excellent system for the examination of potential multiple colonizations of Macaronesia.
|
found Tolpis to be monophyletic and nested within the Lactuceae as a sister group to a large clade containing such genera as Lactuca L., Crepis L., Reichardia Roth, and Dendroseris. Although only five species of Tolpis were included in this study, the Azorean endemic T. azorica was sister to a clade that includes both continental species of Tolpis as well as endemic species from the Canary and Cape Verde archipelagos. This study suggests the intriguing possibility that the extant continental species might be derived from insular species, a pattern opposite to that found by most other studies of Macaronesian endemics. In fact, molecular evidence for continental colonization from Macaronesia is currently restricted to Aeonium Webb & Berthel. (Crassulaceae; Mes, van Brederode, and t'Hart, 1996
).
Tolpis is also interesting for its preponderance of woodiness. Except for the two annual species T. barbata and T. coronopifolia (native to the Mediterranean region and to the Canary Islands, respectively), all members of the genus have woody stems (Jarvis, 1980
). Molecular phylogenetic studies in a variety of island systems, initially in the Hawaiian (Baldwin and Robichaux, 1995
; Givnish et al., 1995
; Wagner, Weller, and Sakai, 1995
) and Juan Fernández Islands (Kim, Crawford, and Jansen, 1996
), have indicated that woodiness typically evolves only after dispersal to the islands, possibly as a result of intense competition for resources in these stable island environments (Carlquist, 1974
; see Givnish [1998]
for a good recent review of insular woodiness and the evidence for the varying hypotheses involved). In contrast, some researchers have historically favored a different view of habit evolution in Macaronesia. Under their hypothesis, woodiness in some Macaronesian endemic plants is a plesiomorphic character, with herbaceous endemics derived from woody ancestors (Lems, 1960
; Meusel, 1965
; Bramwell, 1976
). However, recent molecular phylogenetic analyses have failed to support this evolutionary scenario for Macaronesian plant groups (for examples of Macaronesian groups in which woodiness has been shown to be derived, see Böhle, Hilger, and Martin, 1996
; Kim et al., 1996
; Francisco-Ortega et al., 1997
; Panero et al., 1999
).
For this study, we performed chloroplast DNA (cpDNA) restriction site analyses of Tolpis and four putatively related genera with the following objectives: (1) to examine the pattern of colonization within the island taxa, as well as between the islands and the mainland, and (2) to determine if woodiness is plesiomorphic relative to the extant taxa in the genus.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
. One of the outgroup species, Chlorocrepis staticifolia, has been included within Tolpis by some authors in the past, but both morphology and the ndhF phylogeny indicate that this species is closely allied to Crepis. We have followed Jarvis (1980)
in placing this species in the genus Chlorocrepis. Likewise, both morphological (Jarvis, 1980
) and molecular (Park et al., 2001
) studies allowed us to exclude Hieracium capense L. [formerly treated as Tolpis capensis (L.) Schultz Bip.] from the analysis as well. Finally, we chose to follow Jarvis (1980)
in using the name T. succulenta for plants of both the Azores and Madeira Islands. However, it seems clear from observations in the field, as well as from our cpDNA restriction site data (Fig. 2), that the plants Jarvis and others have referred to this name segregate into two species, one endemic to the Azores and the other to the Madeiran archipelago. We designate these two species T. succulentaAZ and T. succulentaMA, respectively, in this paper. We refrain from giving separate names to either species here due to the considerable nomenclatural confusion surrounding them (Jarvis, 1980
).
|
and was purified in CsCl/ethidium bromide gradients (Sambrook, Fritsch, and Maniatis, 1989
). Cesium purified DNA was digested with 20 restriction enzymes whose recognition sequences varied in length as follows: 11 six base pair (bp) cutters (AseI, AvaII, BclI, BglII, ClaI, DraI, EcoO109I, EcoRI, HincII, NsiI, and XmnI), 2 five bp cutters (BstNI and NciI), and 7 four bp cutters (BstUI, HaeIII, HhaI, HinfI, MspI, RsaI, and TaqI). Two of these enzymes (DraI and TaqI) were subsequently deleted from the analysis due to a high frequency of incomplete DNA digestion. Restriction fragments were separated by agarose gel electrophoresis and bidirectionally transferred to reusable nylon membranes. DNA fragments on these membranes were hybridized to 32P-labelled Lactuca cpDNA probes (Jansen and Palmer, 1987
). Restriction fragments were visualized by exposing the nylon membranes to X-ray film.
Low to moderate levels of restriction site divergence and low levels of fragment length variation enabled the interpretation of fragment patterns without constructing restriction site maps (Jansen, Wee, and Millie, 1998
). If a restriction site gain resulted in fragments too small to be observed, restriction site differences were scored by inferring the presence of small bands. When length variation could not be distinguished from restriction site variation, digest patterns from the same chloroplast region across multiple enzymes were examined in order to ensure that length variants were scored only once.
Restriction site mutations were coded as absent (0) or present (1). The single length change that was detected was scored as the hypothesized ancestral length (0) or derived length (1). The highest level of restriction site variation was observed among the outgroups, such that in a few cases it was difficult to determine the fragment homology among these taxa. In all of these instances the problems in outgroup fragment interpretation did not interfere with determining the corresponding fragment homology within Tolpis. Because our primary interest lay in the phylogeny of Tolpis and not in the relationships among the outgroups, these ambiguities do not affect the conclusions of this paper.
We excluded three samples of Tolpis from the final phylogenetic analyses because their patterns of restriction site variation were identical to those of another sample of the same species. These deleted samples are marked with an asterisk in the voucher table (http://ajbsupp.botany.org). Only parsimony-informative characters were included in the analysis. All parsimony analyses were performed on PAUP* version 4.0b4a (Swofford, 2000
). We performed a heuristic search using 100 random replicates, tree bisection-reconnection (TBR) branch swapping, and MULPARS optimization to find the shortest tree(s). Restriction site gains and losses and length changes were assigned equal weights in the analysis. Clade support was estimated using 10 000 bootstrap replicates (heuristic search using simple addition sequence and MULPARS off; Felsenstein, 1985
). Because the Canary Islands endemic species for which multiple specimens were included in the analysis were polyphyletic (see RESULTS), we tested the monophyly of these species using a constraint tree in which all such species were monophyletic. The significance of the length difference between the resulting tree and the most parsimonious tree was tested using the compare 2 test with 100 replicates (Swofford, 2000
), the Kishino-Hasegawa test (Kishino and Hasegawa, 1989
), and the Templeton test (Templeton, 1983
), as implemented in PAUP* version 4.0b4a. We should note that recent work has called into question the validity of using the Kishino-Hasegawa test to compare topologies that have been specified a posteriori (Goldman, Anderson, and Rodrigo, 2000
). These authors indicate that the only useful result from such a test occurs when the P value rejects the null hypothesis at a level of 0.1 or higher. Because we obtained just such a P value, we chose to include the results of the Kishino-Hasegawa test in the analysis (see RESULTS). Finally, reconstructions of dispersal history and evolution of woodiness were performed using MacClade version 3.03 (Maddison and Maddison, 1992
) with character states treated as unordered and all state changes weighted equally.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The monophyly of Tolpis is supported by a large number of characters (110) and the highest possible bootstrap value (100%). Although restriction site variation within Tolpis is substantially lower than the variation among the outgroup taxa (which may reflect the isolated position that Tolpis may occupy within the Lactuceae), enough variation is present to allow the resolution of several groups within the genus with relatively high support. At least three major clades are evident in the cpDNA phylogeny (Fig. 2): one includes all of the Canary Island endemics along with the single Cape Verde endemic (T. farinulosa), a second includes both Azorean endemic species (T. azorica and T. succulentaAZ), and a third includes both continental species (T. barbata and T. virgata). All three groups are strongly supported by bootstrap values of 100%, 97%, and 91%, respectively. Relationships among these clades and the two species of Tolpis endemic to the Madeira Islands (T. macrorhiza and T. succulentaMA) are also resolved in our phylogeny, although with slightly weaker bootstrap support. The Canary/Cape Verde clade is sister to the two continental species, and this combined clade is sister to the Azorean species (although this combined clade has a lower bootstrap value of 66%). Collectively, this Canary/Cape Verde/continental group is sister to the Madeiran species T. macrorhiza, with moderate bootstrap support (74%). The most basal of all Tolpis species is the other Madeiran endemic, T. succulentaMA. Finally, there is little or no resolution within the large Canary Island/Cape Verde group of species. Only three clades are present within this group under strict consensus, and only one of these has a bootstrap proportion >50% (Fig. 2). All of the Canary Islands species with multiple accessions included in our analysis are polyphyletic. However, constraining these species to be monophyletic results in a tree only five steps longer (298 steps vs. 293 steps). All three topology tests fail to reject the most parsimonious tree as a significantly better fit for the data relative to the constraint tree (P = 0.71 for compare 2 test and P = 0.46 for both the Kishino-Hasegawa and the Templeton tests).
Mapping biogeography onto the cpDNA phylogeny results in nine equally parsimonious reconstructions of dispersal (five steps each) among the archipelagos and the continent. These scenarios are illustrated in simplified form in Fig. 3. The nine reconstructions fall loosely into two groups based on the overall pattern of dispersal history: one of the scenarios (reconstruction 9) requires four separate introductions of Tolpis from the continent to Macaronesia (two dispersals to Madeira, one to the Azores, and one to the Canaries), while the other eight scenarios require initial dispersal of Tolpis from the mainland to the Madeira Islands, followed by extinction of the genus on the continent and subsequent continental recolonization. Within the latter group of reconstructions, there is little agreement as to which archipelago is the source of the existing continental species of Tolpis. Of these eight scenarios, three indicate that a Canary Islands species colonized the continent, three implicate a Madeiran species, and two implicate an Azorean species.
|
|
). Reconstructions of ancient shorelines at the time of the latest glacial maximum (18 000 y ago, when sea levels were 120 m lower than today) document not only that Macaronesian islands were larger and thus slightly closer to each other than at present, but also reveal the existence of several now-submerged islands (García-Talavera, 1999
). A number of these ancient islands lay between the Madeira archipelago and the Iberian peninsula, such that the single greatest overwater distance between Europe and what is now the Madeiran islands was 200 km, rather than the modern 800 km. It is possible that Tolpis may have existed on these islands at some point and perhaps even reached the Madeira archipelago from these submerged islands rather than from elsewhere. However, because no information exists on the fossil floras of these islands, it was assumed that members of Tolpis have not inhabited those islands in the past. Likewise, within some of the Macaronesian archipelagos, Tolpis does not occupy every island available (Jarvis, 1980
). The Canary Islands provide one such example: neither Lanzarote nor Fuerteventura harbor any populations of island endemic Tolpis. Just as in the previous case, it is impossible to determine whether Tolpis ever inhabited these islands due to the lack of fossil evidence. As a result, it was assumed that Tolpis has not occupied these islands in the past, and consequently these two islands were ignored when measuring interarchipelago distances (i.e., the distance between Gran Canaria and the African mainland was used for computing D, rather than the distance between Fuerteventura and the mainland). Finally, because the absolute timing of the dispersal events implied in our reconstructions is unknown, it was assumed that the relative positions of the Macaronesian archipelagos to each other and to Europe and Africa have not changed substantially during the evolution of Tolpis. Thus, in the absence of information on fossil distributions and absolute timing of colonization events, the modern distances between landmasses were utilized in computing D. The lowest overall distance scores occur in reconstructions 1 (D = 2000 km) and 2 (D = 2200 km), which both require continental extinction and recolonization. Reconstruction 9, involving four separate introductions to Macaronesia, has a higher score of 2800 km. In total, six reconstructions score as low or lower than reconstruction 9. The two highest scoring reconstructions (7 and 8) require at least two long-distance dispersal events to or from the Azores.
Finally, ancestral character state reconstruction makes it clear that stem woodiness is plesiomorphic with respect to the extant species of Tolpis (Fig. 2). The topology of the tree in Fig. 2 indicates that the herbaceous annual habit evolved independently in two lineages: one leading to the Canary Islands endemic species T. coronopifolia and the other leading to the widespread continental species T. barbata.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Ranking the nine reconstructions by our minimum distance metric favors the scenarios involving continental extinction and recolonization in Tolpis. Six of these eight reconstructions (1–6 in Fig. 3) have equally as low or lower scores than reconstruction 9, which stands alone in implying four separate Macaronesian invasions. Of these six scenarios, reconstructions 1 and 2 have the lowest overall distance scores. These two scenarios are remarkably similar, differing in only one dispersal event. In reconstruction 1, Tolpis initially colonizes the Madeiran Islands from a now extinct continental ancestor. The Madeiran archipelago then acts as a center of dispersal for the genus: from Madeira, Tolpis independently disperses to the Azores and the Canary Islands. These Canary Islands taxa then colonize the Cape Verde Islands and the continent. Reversing the direction of dispersal from the Canary Islands to the continent (i.e., dispersal directly from Madeira back to the continent and from there to the Canaries) results in reconstruction 2, which only requires an additional 200 km in minimum dispersal distance.
It is clear that the Azores represents the single most influential region in ranking the reconstructions due to the relative isolation of this island group. Because the greatest distances occur between the Azores and the continent and Canary Islands, dispersal events from the Azores to these regions, or vice versa, result in higher distance scores overall. This fact explains why reconstruction 9, which involves a long-distance dispersal event from the continent to the Azores, is outscored by five other reconstructions, none of which requires such a distance to be covered in one event. It also explains why the highest-scoring reconstruction (reconstruction 8) is nearly 1000 km longer than any other: this scenario requires two such long-range dispersals from the Azores. Using dispersal distance as a criterion in our phylogeographic analysis thus seems to favor derivation of the Azorean species of Tolpis from the Madeira Islands, with no further colonization to or from the Azores.
Even though this minimum distance scoring method allows for discerning some general patterns in biogeography, it is difficult to determine which scenario most closely resembles the true colonization history of Tolpis using this metric alone. Aside from geographic distance, factors such as relative landmass sizes and wind currents can also influence the likelihood of being carried from one region to another. For instance, dispersing from a small land mass to a large land mass (i.e., from an island group to a continent) is more likely than the reverse simply because a larger land area presents a larger target for diaspores (MacArthur and Wilson, 1967
). Thus it might be argued that reconstruction 2 should be favored over the similar but lower-scoring reconstruction 1 because, in the former scenario, Madeiran Tolpis disperses first to the large landmass (the continent) and from there to the small landmass (the Canary Islands), rather than the reverse (as seen in reconstruction 1). Likewise, patterns in wind direction could interact with distance to make a given colonization event relatively more or less likely. In Macaronesia, the more southern island groups (the Madeiras, Canaries, and Cape Verdes) are more commonly influenced by northeasterly trade winds than the more northern Azores archipelago, which is subject to mid-latitude westerlies (Leuschner, 1996
). For this reason, even though reconstructions implying long-distance dispersal from the Azores to the Canary Islands or the continent receive high scores due to the great distance between these areas, these scenarios cannot be excluded because the westerly wind currents near the Azores tend to blow diaspores toward these regions naturally (this is not to say that dispersal against the prevailing wind patterns is impossible in Macaronesia; in fact, Panero et al. [1999]
have shown that Pericallis D. Don likely dispersed directly from the Canary Islands to both the Madeira Islands and the Azores). Wind currents such as these may have been particularly important in the dispersal of Tolpis, as the cypselas of many of its members possess long pappus setae (Jarvis, 1980
); these fruits seem well suited for wind dispersal. In view of such confounding factors, it would be premature to select one of the nine reconstructions as closest to the true historical pattern of dispersal in Tolpis.
Even though we cannot fully determine which is correct, each of the nine scenarios, whether involving continental extinction/recolonization, multiple dispersals to Macaronesia, or both, presents a novel pattern of dispersal within the Macaronesian endemic flora. If any of reconstructions 1–8 is true, Tolpis would represent the first documented example of a plant group that successfully recolonized the continent from Macaronesia following extinction. To date, molecular evidence for dispersal of any kind from Macaronesia back to the continent has only been demonstrated in Aeonium (Crassulaceae; Mes, van Brederode, and t'Hart, 1996
). In contrast, Tolpis may have invaded the Atlantic islands four times, as implied by reconstruction 9. This pattern would still be unique among the Macaronesian flora (but not among the Macaronesian biota as a whole; Emerson, Oromí, and Hewitt [2000]
have recently demonstrated that the carabid beetle genus Calathus has invaded Macaronesia at least four times). Molecular studies of other endemic Macaronesian plant groups have revealed that nearly all of these groups result from a single introduction from the mainland (e.g., in Argyranthemum [Francisco-Ortega et al., 1997
]; in the Bencomia Webb & Berthel. alliance [Helfgott et al., 2000
]; in Echium L. [Böhle, Hilger, and Martin, 1996
]; in Sideritis L. [Barber et al., 2000
]; and in the Sonchus alliance [Kim et al., 1996
]). A few groups have been shown to have colonized Macaronesia twice (Ilex [Cuénoud et al., 2000
]; Lavatera [Ray, 1995
; Fuertes-Aguilar et al., in press
]; Olea europaea L. [Hess, Kadereit, and Vargas, 2000
]), while Hedera appears to have invaded this region three times (Vargas et al., 1999
), the most of any group yet studied.
Finally, our data suggest that regardless of the sequence of colonization events within Tolpis, the Cape Verdean endemic T. farinulosa descends from a Canary Islands ancestor. Which of the modern Canary Islands species is most closely related to T. farinulosa cannot be discerned with confidence from the cpDNA restriction site data, however. Because of this ambiguity, it is difficult to determine the specific island within the Canaries that provided the ancestors of T. farinulosa. One shared character unites T. laciniata from the island of El Hierro with T. farinulosa, but this relationship is weakly supported (30% bootstrap value). It should be noted that Jarvis (1980)
hypothesized a close relationship between these same species based on morphological similarity. Even though the exact relationships between T. farinulosa and the Canary Islands species are unresolved, the data clearly place it within this clade. The derivation of T. farinulosa from the Canary Islands is significant biogeographically because it implies a long-distance dispersal event from the Canary to the Cape Verde Islands. The results of the current study add to a growing list of molecular evidence linking the flora of these two archipelagos. Dispersal from the Canary Islands to the Cape Verde Islands has also been implied in molecular phylogenetic studies of Aeonium (Mort et al., in press), Echium (Böhle, Hilger, and Martin, 1996
), and the Sonchus alliance (Kim et al., 1996
).
For the same reasons that it is difficult to place T. farinulosa in the proper context of the Canary Islands endemics, it is also difficult to reconstruct the interisland colonization history of Tolpis within this archipelago. Although the parsimony analysis places all of the Canary and Cape Verde Islands endemics together in a strongly supported monophyletic group, it fails to find any significant grouping of species within this clade. In fact, only one grouping within the entire clade of Canary Island/Cape Verde species (between two specimens of T. laciniata from La Palma) is supported by a bootstrap value >50%. None of the Canary Islands endemic species for which multiple specimens are included in this analysis are monophyletic. However, a constrained parsimony analysis in which all conspecific samples are forced to be monophyletic results in a tree five steps longer (298 steps vs. 293 steps), which is a statistically insignificant length difference. This ambiguity makes it impossible not only to determine the monophyly of these species, but also precludes the reconstruction of any dispersal patterns among the various islands within this archipelago.
The underlying cause of our inability to hypothesize about the sequence and pattern of colonization events in the Canary Islands, i.e., low restriction site variation among the Canary Islands taxa, may indicate the possibility of a relatively recent colonization of the archipelago followed by rapid speciation. Many molecular studies of island plant groups have documented similarly low molecular variation among related island taxa, even in the face of strong morphological divergence (Baldwin et al., 1998
). It is important to mention, however, that variation in the rate of DNA sequence evolution between the Canary Islands clade and the other species of Tolpis may also explain the observed pattern. Perhaps a more variable molecular marker could resolve the relationships, and thereby the colonization history, among these Canary Islands taxa.
Evolution of woodiness
Another consequence of the topology of the cpDNA phylogeny is that woodiness is plesiomorphic in Tolpis (Fig. 2). An evolutionary reduction in woodiness has thus occurred in two separate lineages: once in the Canary Islands (T. coronopifolia) and once on the continent (T. barbata). The annual herbaceous habit in these lineages may have evolved in response to ecological conditions. Both of these species prefer relatively xeric, disturbed environments, in contrast to many of the other island endemics, which typically inhabit the moister upland areas (Jarvis, 1980
). All of the latter species develop woody stems, although their particular growth habits vary (Jarvis, 1980
). That the herbaceous habit displayed by T. coronopifolia and T. barbata likely represents an evolutionary reduction in woodiness seems to be further supported by the fact that both species are able to produce wood under favorable environmental conditions. Jarvis (1980)
reports that T. coronopifolia and T. barbata sometimes behave as biennials, and in such cases woody stem bases occasionally develop.
Although it is difficult to infer the exact sequence of habit evolution from the data, it is clear that woodiness is ancestral in Tolpis and that the herbaceous habit displayed by the annual forms is derived. This type of habit evolution has been documented only once before, in the Macaronesian endemic Crassulaceae. A recent combined molecular/morphological phylogeny of this group strongly suggests that woody island Aeonium gave rise to the herbaceous Canary Islands endemic genus Greenovia Webb in Webb & Berthel. (Mort et al., in press). Recent molecular studies have indicated the opposite pattern (woody habit derived from herbaceous ancestors) to be common in Macaronesia (in Argyranthemum [Francisco-Ortega et al., 1997
]; in Echium [Böhle, Hilger, and Martin, 1996
]; in Ixanthus Griseb. [Thiv, Struwe, and Kadereit, 1999
]; in Pericallis [Panero et al., 1999
]; and in the Sonchus alliance [Kim et al., 1996
]). We should note that our data do not rule out the island derivation of stem woodiness in Tolpis; in fact, they only support the plesiomorphy of this character state with respect to the modern taxa. Because most of the relatives of Tolpis within the Lactuceae are herbaceous, including the four genera we used as outgroups (Bremer, 1994
), it seems obvious that woodiness evolved at some point in the lineage of the last common ancestor of the extant species of Tolpis. Whether this event occurred on the continent or in Macaronesia cannot be determined with current evidence. If the initial colonizers of Tolpis in the islands were in fact woody, and if any of the reconstructions of dispersal history requiring continental extinction and recolonization are accurate, it would imply that the herbaceous continental species T. barbata evolved from woody island ancestors. This type of scenario conforms quite well to the predictions of Meusel, Bramwell, Cronk, and others with respect to the plesiomorphic condition of woodiness in the endemic Macaronesian flora (Lems, 1960
; Meusel, 1965
; Bramwell, 1976
; Cronk, 1992
). They view many of the woody endemics in this region, especially in the humid forests, as relicts of a wider Mediterranean Tertiary flora known from fossil records throughout southern Europe and northern Africa. According to this hypothesis, as the Mediterranean region grew increasingly arid beginning in the late Miocene (Cronk, 1992
), many of these forest taxa were extirpated on the mainland, but survived in Macaronesia (principally in the "laurisilva" of Madeira and the Canary Islands), finding refuge in the stable island climate of these oceanic archipelagos (Meusel, 1965
; Takhtajan, 1969
; Bramwell, 1972, 1976
; Sunding, 1979
; Cronk, 1992
). These researchers further believe that the evolution of herbaceous forms from these island relicts allowed them to recolonize the Mediterranean region. Thus they explain the numerous continental herbaceous relatives of the woody endemic flora of the Atlantic islands.
Most molecular research to date has failed to find any support for these relict hypotheses across numerous Macaronesian plant groups, instead finding that the woody island taxa usually occur in a derived position within their respective phylogenies. The only two examples of probable relictual species that have been documented with molecular data are Lavatera phoenicea Vent. (Malvaceae; Fuertes-Aguilar et al., in press) and Plocama pendula Aiton (Rubiaceae; Bremer, 1996
; Andersson and Rova, 1999
). In neither of these cases, however, can it be shown that these ancient species gave rise to continental descendants. In contrast, Tolpis may be an example of an endemic Macaronesian plant group that has speciated and successfully recolonized the mainland. The two continental species in this genus do in fact occur in a derived position in the cpDNA phylogeny, although it is not certain that these species are descended from island ancestors. Furthermore, it is clear that woodiness is plesiomorphic with respect to modern Tolpis, thus implying that the herbaceous mainland species T. barbata must be derived from woody ancestors. Finally, the ndhF sequence data collected by Park et al. (2001)
indicate a comparatively long branch separating Tolpis from its nearest relatives, suggesting that this genus may represent an isolated lineage within the Lactuceae. If Tolpis was extirpated on the mainland following initial dispersal to Madeira, the resulting geographical restriction of the genus to Macaronesia might explain the observed phylogenetic isolation of this group (and similarly, the relatively long branch leading to Tolpis may indicate a long-term isolation in Macaronesia). For these reasons it seems that Tolpis may conform to the hypothesis that historically isolated, ancestrally woody Macaronesian endemics colonized the mainland in herbaceous form. However, at this point our analysis indicates only a possibility, and we should emphasize that our results were based on a single molecular data set. Further studies are needed to confirm the trends in biogeography and habit that have been suggested by these cpDNA restriction site data.
Conclusions
The colonization history in Tolpis appears to have followed one of two general modes: either the genus dispersed to Macaronesia on four separate occasions, always occupying the adjacent mainland, or it dispersed initially to the Madeira Islands, was extirpated on the continent, and then recolonized Europe and Africa. Which of these scenarios is correct is difficult to determine, although the simple distance metric we employed suggests that Tolpis was indeed extirpated on the continent at some point. Regardless of which reconstruction is correct, however, our cpDNA phylogeny implies that Tolpis dispersed in a novel fashion relative to other Macaronesian plant groups. Our results also indicate that Tolpis is unusual among island plant groups in that woodiness appears to be the ancestral state for all extant taxa in the genus. Finally, reviewing the data for biogeography and woodiness together reveals that Tolpis, unlike other Macaronesian plant groups studied so far by molecular means, may conform to the hypothesis that certain herbaceous Mediterranean plants are derived from woody Macaronesian ancestors. However, for this possibility to prove true, the two extant continental species of Tolpis must be definitively shown to descend from island progenitors.
|
FOOTNOTES |
|---|
5 Author for reprint requests (mjmoore{at}mail.utexas.edu
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Baldwin B. G. D. J. Crawford J. Francisco-Ortega S.-C. Kim T. Sang T. F. Stuessy 1998 Molecular phylogenetic insights on the origin and evolution of oceanic island plants. In D. E. Soltis, P. S. Soltis, and J. J. Doyle [eds.], Molecular systematics of plants II: DNA sequencing, 410–441. Kluwer, Boston, Massachusetts, USA
Baldwin B. G. R. H. Robichaux 1995 Historical biogeography and ecology of the Hawaiian silversword alliance (Asteraceae): new molecular phylogenetic perspectives. In W. Wagner and V. Funk [eds.], Hawaiian biogeography: evolution on a hot spot archipelago, 259–287. Smithsonian Institution Press, Washington D.C., USA
Barber J. C. J. Francisco-Ortega A. Santos-Guerra A. Marrero R. K. Jansen 2000 Evolution of endemic Sideritis (Lamiaceae) in Macaronesia: insights from a chloroplast DNA restriction site analysis. Systematic Botany 25: (4)633-647[CrossRef][ISI]
Böhle U.-R. H. H. Hilger W. F. Martin 1996 Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proceedings of the National Academy of Sciences, USA 93: 11740-11745
Bramwell D. 1972 Endemism in the flora of the Canary Islands. In D. H. Valentine [ed.], Phytogeography and evolution, 141–159. Academic Press, London, UK
Bramwell D. 1976 VI. The endemic flora of the Canary Islands; distribution, relationships, and phytogeography. In G. Kunkel [ed.], Biogeography and ecology in the Canary Islands, 207–240. Dr. W. Junk, The Hague, The Netherlands
Bremer B. 1996 Phylogenetic studies within Rubiaceae and relationships to other families based on molecular data. Opera Botanica Belgica 7: 33-50
Bremer K. 1994 Asteraceae: cladistics and classification. Timber Press, Portland, Oregon, USA
Carlquist S. 1974 Island biology. Columbia University Press, New York, New York, USA
Cronk Q. C. B. 1992 Relict floras of Atlantic islands: patterns assessed. Biological Journal of the Linnean Society 46: 91-103[CrossRef]
Cuénoud P. M. A. Del Pero Martinez P.-A. Loizeau R. Spichiger S. Andrews J.-F. Manen 2000 Molecular phylogeny and biogeography of the genus Ilex L. (Aquifoliaceae). Annals of Botany 85: 111-122
Doyle J. J. J. L. Doyle 1987 A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochemical Bulletin 19: 11-15
Emerson B. C. P. Oromí G. M. Hewitt 2000 Interpreting colonization of the Calathus (Coleoptera: Carabidae) on the Canary Islands and Madeira through the application of the parametric bootstrap. Evolution 54: 2081-2090[ISI][Medline]
Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 46: 159-173
Francisco-Ortega J. D. J. Crawford A. Santos-Guerra R. K. Jansen 1997 Origin and evolution of Argyranthemum (Asteraceae: Anthemideae) in Macaronesia. In T. J. Givnish and K. J. Sytsma [eds.], Molecular evolution and adaptive radiation, 407–431. Cambridge University Press, Cambridge, UK
Fuertes-Aguilar J. M. C. Ray J. Francisco-Ortega A. Santos-Guerra R. K. Jansen In press Molecular evidence from chloroplast and nuclear markers for multiple colonizations of Lavatera (Malvaceae) in the Canary Islands. Systematic Botany.
García-Talavera F. 1999 La Macaronesia: consideraciones geológicas, bigeográficas y paleoecológicas. In J. M. Fernández-Palacios, J. J. Bacallado, and J. A. Belmonte [eds.], Ecología y cultura en Canarias, 41–63. Museo de la Cienca y el Cosmos, Cabildo Insular de Tenerife, Spain
Givnish T. J. 1998 Adaptive plant evolution on islands: classical patterns, molecular data, new insights. In P. R. Grant [ed.], Evolution on islands, 281–304. Oxford University Press, Oxford, UK
Givnish T. J. E. Knox T. B. Patterson J. R. Hapeman J. D. Palmer K. J. Sytsma 1996 The Hawaiian lobelioids are monophyletic and underwent a rapid initial radiation roughly 15 million years ago. American Journal of Botany (Supplement) 83: 159.
Givnish T. J. K. J. Sytsma W. J. Hahn J. F. Smith 1995 Molecular evolution, adaptive radiation, and geographic speciation in Cyanea (Campanulaceae, Lobelioideae). In W. Wagner and V. Funk [eds.], Hawaiian biogeography: evolution on a hot spot archipelago, 299–337. Smithsonian Institution Press, Washington D.C., USA
Goldman N. J. P. Anderson A. G. Rodrigo 2000 Likelihood-based tests of topologies in phylogenetics. Systematic Biology 49: (4)652-670[CrossRef][ISI][Medline]
Hansen A. P. Sunding 1993 Flora of Macaronesia: checklist of vascular plants. 4. Revised edition. Sommerfeltia 17: 1-295
Helfgott D. M. J. Francisco-Ortega A. Santos-Guerra R. K. Jansen B. B. Simpson 2000 Biogeography and breeding system evolution of the woody Bencomia alliance (Rosaceae) in Macaronesia based on ITS sequence data. Systematic Botany 25: 82-97[CrossRef][ISI]
Hess J. J. W. Kadereit P. Vargas 2000 The colonization history of Olea europaea L. in Macaronesia based on internal transcribed spacer 1 (ITS-1) sequences, randomly amplified polymorphic DNAs (RAPD), and intersimple sequence repeats (ISSR). Molecular Ecology 9: 857-868[CrossRef][Medline]
Howarth D. G. D. E. Gardner C. W. Morden 1997 Phylogeny of Rubus subgenus Idaeobatus (Rosaceae) and its implications towards colonization of the Hawaiian Islands. Systematic Botany 22: 433-441[CrossRef][ISI]
Jansen R. K. J. Palmer 1987 Chloroplast DNA from lettuce and Barnadesia (Asteraceae): structure, gene localization, and characterization of a large inversion. Current Genetics 11: 553-564
Jansen R. K. J. L. Wee D. Millie 1998 Comparative utility of chloroplast DNA restriction site and DNA sequence data for phylogenetic studies in plants. In D. E. Soltis, P. S. Soltis, and J. J. Doyle [eds.], Molecular systematics of plants II: DNA sequencing, 87–100. Kluwer, Boston, Massachusetts, USA
Jarvis C. E. 1980 Systematic studies in the genus Tolpis Adanson. Ph.D. dissertation, University of Reading, Reading, UK
Kim S.-C. D. J. Crawford J. Francisco-Ortega A. Santos-Guerra 1996 A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation. Proceedings of the National Academy of Sciences, USA 93: 7743-7748
Kim S.-C. D. J. Crawford R. K. Jansen 1996 Phylogenetic relationships among the genera of the subtribe Sonchinae (Asteraceae): evidence from ITS sequences. Systematic Botany 21: 417-432
Kishino H. M. Hasegawa 1989 Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution 29: 170-179[CrossRef][ISI][Medline]
Lems K. 1960 Floristic history of the Canary Islands. Sarracenia 5: 1-94
Leuschner C. 1996 Timberline and alpine vegetation on the tropical and warm-temperate oceanic islands of the world: elevation, structure, and floristics. Vegetatio 123: 193-206[CrossRef][ISI]
MacArthur R. H. E. O. Wilson 1967 The theory of island biogeography. Princeton University Press, Princeton, New Jersey, USA
Maddison W. P. D. R. Maddison 1992 MacClade, version 3.03. Sinauer, Sunderland, Massachusetts, USA
Mes T. H. M. J. van Brederode H. t'Hart 1996 Origin of the woody Macaronesian Sempervivoideae and the phylogenetic position of the east African species of Aeonium. Botanica Acta 109: 477-491[ISI]
Meusel H. 1965 Die Reliktvegetation der kanarischen Inseln in ihren Beziehungen zur süd-und mitteleuropäischen Flora. In M. Gersch [ed.], Gesammelte Vorträge über moderne Probleme der Abstammungslehre 1, 117–136. Friedrich-Schiller-Universität, Jena, Germany
Mort M. E. D. E. Soltis P. S. Soltis J. Francisco-Ortega A. Santos-Guerra In press Phylogenetics and evolution of the Macaronesian clade (Crassulaceae) inferred from molecular and morphological data. Systematic Botany.
Panero J. L. J. Francisco-Ortega R. K. Jansen A. Santos-Guerra 1999 Molecular evidence for multiple origins of woodiness and a New World biogeographic connection of the Macaronesian Island endemic Pericallis (Asteraceae: Senecioneae). Proceedings of the National Academy of Sciences, USA 96: 13886-13891
Park S.-J. E. J. Korompai J. Francisco-Ortega A. Santos-Guerra R. K. Jansen 2001 Phylogenetic relationships of Tolpis (Asteraceae: Lactuceae) based on ndhF sequence data. Plant Systematics and Evolution 226: 23-33[CrossRef][ISI]
Ray M. F. 1995 Systematics of Lavatera and Malva (Malvaceae, Malveae): a new perspective. Plant Systematics and Evolution 198: 29-53[CrossRef][ISI]
Sambrook J. E. F. Fritsch T. Maniatis 1989 Molecular cloning, a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, New York, USA
Sunding P. 1979 Origins of the Macaronesian flora. In D. Bramwell [ed.], Plants and islands, 13–40. Academic Press, London, UK
Swofford D. L. 2000 PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b4a. Academic Press, Sunderland, Massachusetts, USA
Takhtajan A. 1969 Flowering plants: origin and dispersal. Smithsonian Institution Press, Washington D.C., USA
TBG. 1999 The Times comprehensive atlas of the world, 10th ed. Times Books Group, London, UK
Templeton A. R. 1983 Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37: (2)221-244[CrossRef][ISI]
Thiv M. L. Struwe J. W. Kadereit 1999 The phylogenetic relationships and evolution of the Canarian laurel forest endemic Ixanthus viscosus (Aiton) Griseb. (Gentianaceae): evidence from matK and ITS sequences, and floral morphology and anatomy. Plant Systematics and Evolution 218: 299-317[CrossRef][ISI]
Vargas P. H. A. McAllister C. Morton S. L. Jury M. J. Wilkinson 1999 Polyploid speciation in Hedera (Araliaceae): phylogenetic and biogeographic insights based on chromosome counts and ITS sequences. Plant Systematics and Evolution 219: 165-179[CrossRef][ISI]
Wagner W. L. S. G. Weller A. K. Sakai 1995 Phylogeny and biogeography in Schiedea and Alsinidendron (Caryophyllaceae). In W. Wagner and V. Funk [eds.], Hawaiian biogeography: evolution on a hot spot archipelago, 221–258. Smithsonian Institution Press, Washington D.C., USA
Wendel J. F. A. E. Percival 1990 Molecular divergence in the Galápagos Islands-Baja California species pair Gossypium klotzschianum and G. davidsonii. Plant Systematics and Evolution 171: 99-115[CrossRef][ISI]
Wendel J. F. A. Schnabel T. Seelanan 1995 An unusual ribsomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic intergenomic introgression. Molecular Phylogenetics and Evolution 4: 298-313[CrossRef][ISI][Medline]
This article has been cited by other articles:
|
|
 |
|
  J. K. Archibald, D. J. Crawford, A. Santos-Guerra, and M. E. Mort The utility of automated analysis of inter-simple sequence repeat (ISSR) loci for resolving relationships in the Canary Island species of Tolpis (Asteraceae) Am. J. Botany, August 1, 2006; 93(8): 1154 - 1162. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Moore, A. Tye, and R. K. Jansen Patterns of long-distance dispersal in Tiquilia subg. Tiquilia (Boraginaceae): implications for the origins of amphitropical disjuncts and Galapagos Islands endemics Am. J. Botany, August 1, 2006; 93(8): 1163 - 1177. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Crawford, J. K. Archibald, A. Santos-Guerra, and M. E. Mort Allozyme diversity within and divergence among species ofTolpis(Asteraceae-Lactuceae) in the Canary Islands: systematic, evolutionary, and biogeographical implications Am. J. Botany, April 1, 2006; 93(4): 656 - 664. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Lee, S.-C. Kim, K. Lundy, and A. Santos-Guerra Chloroplast DNA phylogeny of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian Islands Am. J. Botany, December 1, 2005; 92(12): 2072 - 2085. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Lahaye, L. Civeyrel, T. Speck, and N. P. Rowe Evolution of shrub-like growth forms in the lianoid subfamily Secamonoideae (Apocynaceae s.l.) of Madagascar: phylogeny, biomechanics, and development Am. J. Botany, Augu |
); woody taxa are indicated by a closed square (
). An evolutionary change from an herbaceous to a woody habit along a branch is indicated by a closed circle (
); a change from a woody to an herbaceous habit along a branch is indicated by an open circle (
)