American Journal of Botany 94(4): 625–639. 2007.
DOES MACARONESIA
EXIST?
CONFLICTING
SIGNAL IN THE
1
BRYOPHYTE AND PTERIDOPHYTE FLORAS
A. VANDERPOORTEN,2,3 F. J. RUMSEY,4
2
AND
M. A. CARINE4
Institute of Botany, University of Liège, B22 Sart Tilman, Liège, Belgium; and 4Department of Botany,
The Natural History Museum, Cromwell Road, London, SW7 5BD, UK
Macaronesia, which includes five mid-Atlantic archipelagos (Azores, Madeira, Selvagems, Canaries, and Cape Verdes), has
been traditionally recognized as a distinct biogeographic unit whose circumscription has been intimately associated with the
hypothesis that the flora is a relict of a formerly broadly distributed subtropical Tertiary flora. The concept of Macaronesia is
revisited here using parsimony and Bayesian analyses of floristic data sets for the moss, liverwort, and pteridophyte floras. All
analyses reject the monophyly of Macaronesia s.l., resolving the Cape Verdes with tropical Africa. Of the other Macaronesian
archipelagos, the liverwort and pteridophyte analyses support, or could not reject, an Azorean-Madeiran-Canarian clade (hereafter
Macaronesia s.s.), but the moss analysis resolves the Canary Islands as sister to North Africa, thus rejecting the concept of
Macaronesia s.s. for this group. Dynamic interchange of taxa with neighboring continental areas rather than relictualism best
explains the relationships of the Cape Verde cryptogamic flora and the Canary Island moss flora. In contrast, relictualism is
consistent with a monophyletic Macaronesia s.s. for liverworts and pteridophytes. However, from the limited information
available on relationships of endemic cryptogams, this explanation alone may be unsatisfactory. Spatially congruent patterns may,
in fact, conceal a complex mixture of relictual distributions and more recent speciation and dispersal events.
Key words:
biogeography; dispersal; Macaronesia; parsimony analysis of endemicity; refugia; relictualism.
Oceanic islands have been intimately associated with the
study of evolution since Darwin’s theory of evolution by
natural selection in Galapagos finches (Emerson and Kolm,
2005). Islands indeed represent discrete geographical entities
isolated by oceanic barriers that reduce genetic interchanges
with continental areas. Islands are furthermore often characterized by rapid and dramatic ecological changes resulting from
a geological dynamic associated with historical and contemporary volcanic and erosional activity. Altogether, these factors
have promoted fast rates of endemic speciation, making islands
ideal natural laboratories for the study of evolution (Emerson,
2002; Emerson and Kolm, 2005). Typical examples of island
model systems include the Galapagos, Hawaii, and Macaronesia, an array of mid-Atlantic volcanic islands including the
Azores, Madeira, Selvagems, Canaries, and Cape Verdes
situated in the North Atlantic Ocean between 158 and 408 N
(e.g., Hansen and Sunding, 1993) (Fig. 1).
Several early authors alluded to the fact that the floras of the
Macaronesian archipelagos differ from those of nearby
continental areas (e.g., Webb and Berthelot, 1836–1850; see
Lobin, 1982 for a review), but Engler (1879) was the first to
use the term Macaronesia and was also the first to recognize a
distinct biogeographic unit comprising the Azores, Madeira,
and the Canaries. Later authors expanded the circumscription
of the region to include also the Cape Verdes (e.g., Dansereau,
1961; Takhtajan, 1969; Bramwell, 1972, 1976) and, in some
cases, continental enclave areas in North Africa and Iberia,
where species with Macaronesian affinities occur (Sunding,
1979).
The delimitation of Macaronesia by Engler (1879) and
1
subsequent authors (e.g., Dansereau, 1961; Takhtajan, 1969;
Bramwell, 1972, 1976; Sunding, 1979) placed particular
emphasis on the endemic element of the vascular flora. This
element constitutes approximately 20% of vascular plant
species overall (Humphries, 1979) and accounts for almost
two-thirds of the native Canarian (González Martı́n and
González Artiles, 2001) and Azorean (Schäfer, 2003) floras,
respectively. Endemic taxa considered characteristic of the
region include several Lauraceae species (e.g., Laurus azorica,
Apollonias barbujana, Persea indica, and Ocotea foetens),
other taxa that are widespread within the region (e.g.,
Dracaena draco subsp. draco), and distinctive Macaronesian
endemic groups that have undergone extensive intraregional
radiation, such as the endemic genus Argyranthemum and
Macaronesian Echium (e.g., Takhtajan, 1969). Engler (1879)
proposed that this distinctive endemic element of the
Macaronesian flora was, for the most part, a relict of a
formerly widespread subtropical flora that covered southern
Europe and North Africa during the Tertiary (hereafter the
Engler refugium model). This hypothesis was later supported
by Takhtajan (1969), Bramwell (1972, 1985), and Sunding
(1979) among others; i.e., those authors who also promoted the
concept of the Macaronesian region. Despite considerable
variation in age (ranging from 0.04 Myr [Azores] to 24–27 Myr
[Selvagems], in altitude (from 154 m [Selvagems] to 3718 m
[Canaries; Fernández-Palacios and Dias, 2001]), climate,
ecology, and floristic composition across the archipelagos
(see Fernández-Palacios and Dias, 2001), the Macaronesian
concept has been generally widely accepted and the region is
recognized as an important floristic area for conservation
within the European-Mediterranean climate region (Médail and
Quézel, 1997).
Several recent authors addressing the relationships of the
Macaronesian archipelago floras have, however, implicitly
challenged the concept of Macaronesia by classifying the floras
of the different archipelagos in different biogeographic regions.
For example, Rivas-Martinez et al. (2004) included the Azores
Manuscript received 16 June 2006; revision accepted 26 February 2007.
This research was initiated at the Natural History Museum in the context
of the EEC Synthesys exchange program. Many thanks are due to R.
Schumacker and two anonymous referees for their constructive comments
on a first draft of this paper. A.V. acknowledges financial support from the
Belgian Funds for Scientific Research.
3
Author for correspondence (e-mail: a.vanderpoorten@ulg.ac.be)
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Fig. 1.
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Map of the north Atlantic showing the positions of the Macaronesian archipelagos.
within the Euro-Siberian region, and Madeira and the Canaries
within the Mediterranean region (the Cape Verdes were not
considered). Lobin (1982) placed the Azores within the
submediterraean subregion, the Canaries and Madeira with
western Morocco within a Canarian-Mediterranean subregion,
and the Cape Verdes within the ‘‘Saharo-sindian’’ region.
Lobin’s classification utilized both the endemic and the native,
non-endemic elements of the flora, an approach that is in
marked contrast to the exclusive emphasis on the endemic
element by Engler and other proponents of the Macaronesian
concept. Indeed, it is more closely related to dispersalist island
biogeographic models, emphasizing the interchange of species
between continental and island areas that were first developed
by Wallace (1881) for the Macaronesian archipelagos.
Hereafter, we refer to this concept as the dynamic interchange
model.
Paleogeographical and paleontological data do not provide
irrefutable evidence for the Engler refugium model. Terrestrial
plant fossils dated at 13 myr BP have been recorded from Gran
Canaria, and fossils of several plant taxa that are currently
restricted to or have distributions centered on Macaronesia
have been discovered in continental Europe (Sunding, 1979;
Frahm, 2004). These would certainly support a previously
more widespread distribution for the taxa concerned, thus
supporting the relict theory. In many instances, however, the
identification of such fossil material is inconclusive (Garcı́a-
Talavera et al., 1995). Recent dating studies have shown that
some of the 20 large volcanic sea mounts located between the
Canary Islands, Madeira, Selvagems, and the continent, several
of which are presently less than 100 m below sea level, are at
least 68 myr old (Geldmacher et al., 2001). It is conceivable
that they may once have formed aerial islands, facilitating the
migration of species from the continent to the islands during
favorable periods and prior to continental extinction events
(Garcı́a-Talavera, 1997).
Recent molecular phylogenetic evidence further suggests
that the patterns of relationship and evolution of the
Macaronesian endemic vascular flora are much more complex
than the Engler refugium model would predict (see Emerson,
2002; Carine et al., 2004; and Carine, 2005 for a review). In
light of such changing views on the evolutionary history of the
region’s flora and because the circumscription of the region (a
pattern) and the Engler refugium model (an explanatory
hypothesis) have been so intimately linked, a critical reevaluation of the concept of Macaronesia is necessary.
To date, and despite considerable debate concerning the
relationships of the Macaronesian archipelago floras, consideration of the Macaronesian concept has lacked an explicit
analytical framework. de Nicolás et al. (1989) presented a
phenetic study of relationships of the vascular floras within the
Macaronesian region and highlighted the similarities between
the Canarian and Madeiran floras and the distinctiveness of
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V ANDERPOORTEN
ET AL .—D OES
both the Azorean and Cape Verdean floras. However, no
continental areas were included in the analysis, and it was
consequently not possible to explicitly test the circumscription
of the Macaronesian region. Furthermore, a large number of
non-native taxa (estimated at between 41–49% of the Canarian
flora; González Martı́n and González Artiles, 2001) were
included in the analysis. This element of the flora introduces a
substantial bias into the analysis, obscuring the signal from the
native flora.
The debate concerning the Macaronesian concept has also
focussed principally on the flowering plant flora. The
cryptogamic, and particularly the bryophyte floras, have
received much less attention, even though in terms of numbers
and biomass they contribute a significant component to these
insular ecosystems. The existence of a number of cryptogamic
taxa of African (Manton et al., 1986) and American (Britton
and Brunton, 1996; Schäfer, 2001) origin has long been
acknowledged, but hypotheses to explain the origins of the
Macaronesian cryptogamic flora have typically followed the
Engler relictualism model, with the flora of the region
considered a relict species pool from the European Tertiary
flora (Gibby, 1979; Manton et al., 1986; Frahm, 2005).
Examples of putative Macaronesian relicts include the fern
Woodwardia radicans, which is presently disjunctly distributed
in Macaronesia, the Iberian peninsula, Corsica, Italy, and Crete,
but which is also known from Pliocene deposits in France
(Gibby, 1979; Manton et al., 1986), and the moss genus
Echinodium, currently known only from Macaronesia and
Australasia but also known from Baltic and Saxon amber
fossils (Eocene, 37–57 Myr BP) (Frahm, 2004). As with
angiosperms, however, the generality of this explanatory model
has been challenged both by recent re-interpretation of
phytogeographic patterns (Schumacker, 2001) and by molecular phylogenetic evidence that, although still extremely
limited (Rycroft et al., 2004; Vanderpoorten and Long,
2006), suggests that at least some elements of the Macaronesian cryptogamic flora are of much more recent origin than
previously thought.
In this paper, we analyze relationships of the Macaronesian
bryophyte (moss and liverwort) and pteridophyte floras in a
worldwide context. Two methods were used to provide an
explicit analytic framework for this study: parsimony analysis
of species assemblages (PASA, Trejo-Torres and Ackerman,
2002), broadly comparable to the parsimony analysis of
endemicity approach (PAE) of Morrone (1994), and a
maximum likelihood (ML) model of species gains and losses
(Lewis, 2001) implemented within a Bayesian context.
As opposed to more traditional clustering techniques such as
UPGMA, which examine overall extant floristic relationships
among areas without taking similarities due to common
ancestry into account, cladistic methods attempt at grouping
areas into ‘‘monocladic’’ groups, which can be attributed to a
common hypothetical factor and which are characterized by
shared species (Trejo-Torres and Ackerman, 2002). The power
of PAE (and thus related approaches including PASA) to
recover the history of colonization has, however, been
questioned because important information on the history of
biota contained in the cladistic relationships among taxa is not
taken into account (Humphries, 2000; Brooks and van Veller,
2003; Santos, 2005). While it has been suggested that the
parsimony criterion may implicitly favor certain mechanisms
as a possible explanation for the resulting biogeographic
patterns (Santos, 2005), cladistic approaches nonetheless
M ACARONESIA
EXIST ?
627
remain a potentially useful tool for identifying areas designated
by species with congruent distributions (Garcia-Barros et al.,
2002) and have a series of attractive features for ecological
studies of composition patterns. PASA is arguably a more
unified tool when compared to the numerous clustering
algorithms, which can return conflicting results, and also
appears as a more conservative approach. While clustering
techniques produce fully resolved dendrograms, cladistic
analyses can indeed result in unresolved relationships when,
for example, conflicting patterns are found in equally
parsimonious trees (Trejo-Torres and Ackerman, 2001,
2002). In addition, the robustness of the conclusions drawn
from a cladistic analysis can be easily assessed through
statistics such as the bootstrap or the jackknife. Although it is
possible to use these procedures in distance-based methods,
they are rarely utilized for ecological studies and are actually
not implemented in most ecological analysis sofwares. Finally,
and perhaps most importantly in the context of the present
study, the significance of competing explanatory hypotheses
can be statistically evaluated when model-based approaches are
utilized. Specifically, these techniques are used here to
determine which of the Engler relictualism model (consistent
with a monophyletic Macaronesia) and dynamic interchange
model (consistent with a polyphyletic Macaronesia with each
archipelago most closely related to the near continent) provides
a better representation of the observed floristic patterns for the
three studied groups.
MATERIALS AND METHODS
Distribution data—Among bryophytes, only the mosses and liverworts
were analyzed; the six species of hornwort recorded from the Macaronesian
region were not included in the analyses. Indeed, the hornworts represent an
independent group (Shaw and Renzaglia, 2004), which, for consistency, should
be analyzed separately. However, the number of species did not warrant a
separate analysis.
Distributions of mosses, liverworts, and pteridophytes were analyzed for
each Macaronesian archipelago, i.e., the Azores (Az), Madeira (Mad), Canaries
(Can), and Cape Verdes (CV), with the exception of the Selvagems. The
cryptogamic flora of the Selvagems has not been well researched, although,
with a total surface area of ca. 4 km2, a strong marine influence, and little
habitat diversity, the very low species diversity recorded is probably an
accurate reflection of the flora. This depauperate assemblage is of
predominantly widespread saline-tolerant taxa, which reveal little with regard
to the biogeographic issues being tested.
Extra-Macaronesian distributions for all taxa were recorded following the
floristic regions recognized by Hollis and Brummitt (1992), namely Europe
(EUR), northern Africa (AF1), continental sub-Saharan Africa (AF2),
Mascarene Islands (AF3), southern Africa (AF4), northern Asia (AS1), central
Asia (AS2), southern Asia (AS3), southwestern Asia (AS4), western Asia
(AS5), North America (AM1), Central America (AM2), Caribbean islands
(AM3), northern South America (AM4), Brazil (AM5), southern South
America (AM6), Australia (AU1), New Zealand (AU2), Antarctica (ANT),
and Oceania (OC).
The sources for all the distribution data are listed in Appendix S1 (see
Supplemental Data accompanying online version of this article). Twenty
pteridophyte taxa, introduced, or thought to be introduced, into the archipelagos
were excluded. The majority of these are cultivated ornamentals, many of
which have become widely naturalized. For the Australasian or Asian taxa, it is
easier to conclude an origin through garden sources as more plausible than wide
disjunctions, but arguably some neotropical taxa, e.g., Adiantum raddianum, or
more broadly distributed pantropical weedy taxa that were excluded, could be
natural colonists. Judgement on these is, by necessity, subjective, but a
restriction to disturbed areas close to habitation and the recent discovery dates
were considered grounds for their exclusion. Some taxa previously considered
to be introduced, e.g., Selaginella kraussiana, have now been shown from
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palynological studies to have been present prior to human settlement (H.
Schäfer, University of Munich, personal communication).
Nomenclature follows Grolle and Long (2000) for liverworts and Hill et al.
(2006) for mosses except in Leucobryum, as Hill et al.’s treatment has
important phytogeographic consequences that are at odds with recent molecular
and morphological evidence (Vanderpoorten et al., 2003). For pteridophytes,
nomenclature follows Tutin et al. (1993), Lobin et al. (1998), and Press and
Short (1994), with the exception of the treatment of the Asplenium ceterach
complex, more recently elucidated by Van den Heede et al. (2004), and
Polypodium. The taxonomy of the latter is controversial and, as yet, unresolved.
Some authors recognize the Azorean plants as a species distinct from the
Madeiran/Canarian taxon (e.g., Schäfer, 2001), and regard both as distinct at
specific level from the European P. cambricum, whereas others sink all of the
island plants into P. cambricum but as a distinct subspecies (e.g., Neuroth,
1996). On the balance of available information, we have chosen to adopt an
approach between these extremes.
Data analysis—Parsimony—Under MP, a cladistic analysis of the species
3 areas data matrix was conducted to find the most parsimonious classifications
for each group. All analyses included an all-zero outgroup to allow topologies
to be rooted (Morrone, 1994; Trejo-Torres and Ackerman, 2002). Parsimony
analyses were performed using PAUP* beta version 4.0b5 (Swofford, 2002).
Each data set was analyzed using a heuristic search comprising 1000 random
replicate searches with ACCTRAN, MULPARS, and tree-bisection-reconnection (TBR) options. The equally parsimonious trees from each analysis were
summarized into a strict consensus tree that was used to examine the
relationship of each archipelago. Support for clades was assessed by computing
decay values (BS; Bremer, 1988).
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two optimizations returned conflicting states at a node, the state was termed as
ambiguous. Only species with non-ambiguous reconstructions of ancestral
distributions at the node of interest were considered.
Support for the reconstructions was assessed by calculating the relative
probabilities of presence and absence of a species at each internal node using
the ML optimization across the Bayesian sample of trees. The use of an ML
model of species gains and losses for reconstructing ancestral distribution areas
is complementary to the more traditional MP optimization because it provides
an estimate of the confidence in the reconstructions at each node within a tree
(Cunnigham, 1999). We implemented the model of Lewis (2001), which
assumes identical forward and backward transition rates, to find the rate value
that maximizes the probability of the data given the model. The rate parameter
was then fixed and the set of ancestral state probabilities derived for each
internal node. These settings correspond to the ‘‘global’’ approach as described
by Schluter et al. (1997), Pagel (1999), and Mooers (2004). If the difference in
log-likelihood of the two states at a node was .2, the state with the lower
likelihood was rejected. Otherwise, the reconstruction was considered as
ambiguous at the node. This was performed for each tree including the node of
interest to take phylogenetic uncertainty into account. The results of all trees
were then combined to form the full range of probabilities of ancestral character
states at a node across trees, as implemented by Mesquite. This technique
provides an approximation, in a statistical sense, of the probability distribution
of states at a node. Reconstruction can be considered well supported if they
appear in .95% of the sampled trees. Hereafter, we use the term BaSP value
(Bayesian sample proportion) to refer to the percentage of trees in the Bayesian
sample, for which a reconstruction was significantly supported.
RESULTS
Maximum likelihood—The model of Lewis (2001), which employs equal
forward and backward transition rates that can be interpreted in terms of
immigration and extinction rates in the present context, was implemented
within a Bayesian context to sample phylogenies and model parameters
according to their posterior probabilities. Three Markov Chain Monte Carlo
(MCMC) of 5 000 000 iterations each were run in MrBayes 3.0 (Huelsenbeck
and Ronquist, 2003), and trees were sampled every 10 000 generations to
ensure independence of successive trees. The number of generations needed to
reach stationarity in the Markov Chain Monte Carlo algorithm was estimated
by visual inspection of the plot of the ML score at each sampling point. The
trees of the ‘‘burnin’’ for each run were excluded from the tree set, and the
remaining trees from each run were combined to form the full sample of trees
assumed to be representative of the posterior probability distribution. A 50%
majority-rule consensus tree was constructed in PAUP* and rooted using an allzero outgroup.
Constraint analyses were performed to test whether the data rejected a
monophyletic concept of Macaronesia in a broad sense, i.e., including the Cape
Verdes, Madeira, Canaries, and Azores (hereafter, Macaronesia s.l.), or in a
narrower sense, i.e., with the Cape Verdes excluded (hereafter, Macaronesia
s.s.). Significant departure of alternative topologies involving a monophyletic
Macaronesian concept from the optimal topologies was tested by constraining
the Macaronesian archipelagos to monophyly. Under MP, usual tests such as
Kishino and Hasegawa (KH; 1989) were shown to be strongly biased when the
trees compared are not derived independently of the data sets used for testing
(Goldman et al., 2000). The results returned by an uncorrectly applied KH test
only hold if the associated p value is greater than twice the value required to
indicate no rejection of the null hypothesis. If the p value is less than this, it is
impossible to determine from the KH test what the result would be for any test
making proper allowance for a posteriori selection of hypotheses (Goldman et
al., 2000). Modified tests, such as that of Shimodaira and Hasagawa (1999), are
presently only implemented under the ML criterion. Therefore, competing
hypotheses regarding the monophyly of Macaronesia were only tested under
ML within a Bayesian framework. For that purpose, the Bayesian analyses
described were re-run under the constraint of a monophyletic Macaronesia
(both sensu lato and sensu stricto). Differences in average ln L returned by the
constrained and unconstrained analyses were compared using a z test.
Taxon optimizations—To identify taxa (or the shared absence of taxa)
supporting groupings in each of the analyses, we used the MP criterion to
reconstruct ancestral states (i.e., presence or absence of taxa) onto the strict
consensus tree of the MP analysis. Both uppass and downpass optimizations
(Cunningham et al., 1998) were determined for nodes of interest on the strict
consensus tree using Mesquite 1.06 (Maddison and Maddison, 2005). When the
Pteridophytes—The pteridophyte data matrix (Appendix S1
and S2; see Supplemental Data accompanying online version
of this article) comprises 102 taxa. One thousand four hundred
eighty trees were sampled during the Bayesian procedure after
convergence of the three independent Markov chains. Macaronesia in a broad sense is not monophyletic (Fig. 2). The
Azores and Madeira are resolved as sisters within a clade with
a 99% posterior probability. The Canaries are resolved as sister
to the Azores þ Madeira clade to form a Macaronesian s.s.
clade that appears in 65% of the sampled trees. Macaronesia
s.s. is sister to Europe, with which it forms a clade present in all
sampled trees. This clade is included within a larger, nesting
clade (posterior probability ¼ 100%), which also includes
northern Africa (AF1) and western Asia (AS5) and is hereafter
termed the EurAsAf clade. The Cape Verdes belong to a
distinct and distantly related sub-Saharan African clade with
posterior probability of 98%, within which the archipelago is
resolved as sister to continental tropical Africa (AF2; posterior
probability ¼ 71%). Constraining the Markov chains to only
sample trees that fit with a monophyletic Macaronesian
concept resulted in topologies that displayed significantly
lower average ln L values (P , 0.001). Therefore, a broad
Macaronesian concept that would include the Cape Verdes,
Canaries, Azores, and Madeira, can be rejected.
The parsimony analysis, which included 82 informative
characters, resulted in 38 most parsimonious trees of length
228 steps (CI ¼ 0.443; RI ¼ 0.673). The topology of the strict
consensus tree is similar to that derived from the Bayesian
analysis, albeit somewhat less resolved. The Azores and
Madeira are resolved as sister taxa (BS ¼ 3), within a
trichotomy that also includes the Canary Islands and Europe
(BS . 5). North Africa is resolved as sister to this clade (BS .
5). The Cape Verde Islands are resolved in a trichotomy with
sub-Saharan Africa (BS ¼ 2).
Taxa unambiguously optimized onto nodes of interest in the
parsimony strict consensus tree under the MP criterion,
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V ANDERPOORTEN
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together with support for the reconstructions under the ML
criterion across the Bayesian tree sample, are listed in Table 1.
The inclusion of the Cape Verdes within a sub-Saharan clade
is supported by 21 synapomorphic species occurrences, nine of
which have BaSP values significant at the 95% level under the
ML criterion and four of which are restricted to sub-Saharan
Africa. The shared absence of Botrychium lunaria (BaSP ¼
99%) is also characteristic for the sub-Saharan African clade.
Within the sub-Saharan Africa clade, the Cape Verdes lack
any endemic pteridophyte species but are characterized by
homoplastic species occurrences that correspond to disjunct
distribution patterns. Asplenium aethiopicum subsp. braithwaitii and Dryopteris oligodonta have a homoplastic distribution
that spans the Azores-Madeira clade and/or the Canaries and
the Cape Verdes and are the only two elements that can be
regarded as endemic to Macaronesia s.l. Four taxa found in the
Cape Verdes (Pteridium aquilinum subsp. aquilinum, Asplenium hemionitis, Diplazium caudatum, and Davallia canariensis) are also distributed in the EurAsf clade but are not found
elsewhere within sub-Saharan Africa.
Under the MP criterion, the inclusion of Macaronesia s.s.
within EurAsAf and its two nested clades [the first excluding
western Asia (AS5) and the second excluding northern Africa
(AF1)] is characterized by the shared occurrences of 16 species
endemic to the clade. The shared presence of another 15 nonendemic species further characterizes EurAsAf and its nested
clades. Seventeen of the 31 taxa supporting this clade under the
MP criterion are also supported by BaSP values of .95%
under ML.
Macaronesia s.s., which is resolved in the Bayesian analyses
and in 50% of the MP trees, is supported by the endemic
Asplenium anceps and three further non-endemic species. The
latter represent homoplastic occurrences of sub-Saharan
African (Selaginella kraussiana and Adiantum reniforme) and
pantropical (Asplenium monanthes) species. Two synapomorphic absences further characterize the Macaronesia s.s. clade.
None of the taxa supporting this clade have BaSp values of
.95% under the ML criterion.
Within Macaronesia s.s., the Canaries, which are sister to the
clade formed by the Azores and Madeira, are characterized by
the autapomorphic occurrence of four endemic species (Table
4) and the homoplastic presence of Grammitis quaerenda, a
sub-Saharan African species that is nowhere else present within
EurAsAf. The sistership of the Azores and Madeira is
significantly supported under ML by the synapomorphic
presence of four endemic and four other synapomorphic
presences of non-endemic species. All have BaSp values of
,95%. The clade comprising Madeira and the Azores is also
characterized by the synapomorphic absence of eight species
under MP, all of which have BaSp values of ,95% under ML.
The Azores and Madeira each have a suite of specific
autapomorphic endemic species that are listed in Table 4. The
Azores are furthermore characterized by the homoplastic
occurrence of four taxa, namely Ceradenia jungermannioides,
Grammitis marginella, Pityrogramma calomelanos var. calomelanos, and P. ebenea, which have an otherwise American
distribution.
Mosses—The moss data matrix (Appendix S1 and S3; see
Supplemental Data accompanying online version of this article)
comprises 479 taxa. In keeping with the pteridophyte analysis,
the Macaronesian archipelagos do not form a monophyletic
group in the 50% majority-rule consensus tree of the 1279 trees
M ACARONESIA
EXIST ?
629
Fig. 2. Phytogeographic affinities of the Macaronesian pteridophyte
flora inferred from a 50% majority-rule consensus of 1480 trees sampled
after convergence of three independent Markov chains implementing a
model of equal transition rates. Branch lengths were averaged over the
1480 trees. Numbers below the branches correspond to their posterior
probabilities. Shaded clades correspond to the EurAsAf clade and the subSaharan African clade discussed in the text. Numbers above the branches
of those clades are the Bremer supports. Area codes are as follows: Az,
Azores; Mad, Madeira; Can, Canaries; CV, Cape Verdes. Area codes
outside Macaronesia follow Hollis and Brummitt (1992): Eur, Europe;
AF1, northern Africa; AF2, continental sub-Saharan Africa; AF3,
Mascarene Islands; AF4, southern Africa; AS1, northern Asia; AS2,
central Asia; AS3, southern Asia; AS4, southwestern Asia; AS5, western
Asia; AM1, North America; AM2, Central America; AM3, Carribean
islands; AM4, northern South America; AM5, Brazil; AM6, southern
South America; ANT, Antarctica; OC, Oceania; AU1, Australia; AU2,
New Zealand.
sampled during the Bayesian procedure (Fig. 3). The Cape
Verdes are included within a sub-Saharan African clade
(posterior probability ¼ 84%) and within this clade are resolved
as sister to the Mascarene Islands (AF3) (posterior probability
¼ 72%). The remaining Macaronesian archipelagos of the
Canaries, Azores, and Madeira are included within the
EurAsAf clade (posterior probability ¼ 100%). Within the
latter, the Azores and Madeira are resolved as sister areas
(posterior probability ¼ 99%), and this clade is resolved as
sister area to Europe (posterior probability ¼ 83%). The
Canaries are resolved in a different subclade clade within
EurAsAf that also includes northern Africa and western Asia
(posterior probability ¼ 91%). Within this subclade, the
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TABLE 1. Synapomorphic pteridophyte species gains and losses of Macaronesian archipelagos and nesting clades. All reconstructions are based on a
maximum parsimony (MP) optimization onto the strict consensus of the MP analysis. Asterisks indicate that the reconstruction was significant under
maximum likelihood (ML) in .95% of the trees from the Bayesian sample. Endemic synapomorphic transitions are in boldface.
Clade
Cape Verdesþsub-Saharan Africa
EurAsAf, (Madeira-Azores–Canaries-EUR-AF1),
and (Madeira-Azores–Canaries-EUR)
MadeiraþAzoresþCanariesa
MadeiraþAzores
a
Synapomorphies
Gains: Actiniopteris radiata*, Adiantum capillus-veneris, A. incisum*, A. philippense*, A. reniforme,
Asplenium adiantum-nigrum, A. monanthes, A. trichomanes subsp. quadrivalens, Cosentinia vellaea
subsp. vellea, Cystopteris diaphana, Dryopteris pentheri*, Equisetum ramosissimum, Hypodematium
crenatum*, Marsilea coromandeliana*, Nephrolepis undulata*, Ophioglossum lancifolium*, O.
polyphyllum, O. reticulatum, Pellaea viridis*, Selaginella kraussiana, Stegnogramma pozoi.
Losses: Botrychium lunaria*.
Gains: Asplenium adiantum-nigrum, A. hemionitis*, A. obovatum subsp. lanceolatum*, A. onopteris*,
A. scolopendrium*, Blechnum spicant*, Cheilanthes guanchica*, C. tinaei, Christella dentata, Culcita
macrocarpa*, Davallia canariensis, Diplazium caudatum, Dryopteris affinis subsp. affinis*, D.
guanchica, Equisetum ramosissimum, E. telmateia*, Hymenophyllum tunbrigense, H. wilsonii*,
Lycopodiella inundata, Marsilea quadrifolia, Ophioglossum azoricum*, Oreopteris limbosperma,
Pellaea viridis*, Psilotum nudum, Pteridium aquilinum subsp. aquilinum*, Pteris incompleta*,
Selaginella denticulata*, S. selaginoides, Stegnogramma pozoi, Trichomanes speciosum*,
Woodwardia radicans*.
Losses: Actiniopteris radiata, Adiantum incisum*, Hypodematium crenatum, Marsilea coromandeliana.
Gains: Selaginella kraussiana, Adiantum reniforme, Asplenium anceps, A. monanthes.
Losses: Lycopodiella inundata, Psilotum nudum.
Gains: Asplenium reniforme, A. lolegnamense, Diphasiastrum madeirense, Elaphoglossum
semicylindricum, Huperzia dentata, H. suberecta, Notholaena marantae, Pityrogramma calomelanos
var. aureoflava.
Losses: Asplenium ceterach subsp. ceterach, Cystopteris dickieana, Dryopteris guanchica, Marsilea
quadrifolia, Ophioglossum polyphyllum, Polystichum aculeatum, Salvinia natans, Selaginella
selaginoides.
Clade collapsed on the strict consensus in the MP analyses and reconstructions only based on the Bayesian sample of trees under the ML criterion.
Canaries are resolved as sister to northern Africa (posterior
probability ¼ 81%).
Constraining the Markov chains to only sample trees that
include a monophyletic group comprising either all four
Macaronesian archipelagos or Macaronesia s.s. (i.e., Canaries,
Azores, and Madeira) resulted in topologies that displayed
significantly lower ln L values (P , 0.001 in both cases).
Therefore, both a broad and narrow Macaronesian concept can
be rejected.
Analysis of the 446 informative characters under the MP
criterion resulted in eight equally parsimonious trees of length
1616 steps (CI ¼ 0.297; RI ¼ 0.596). The strict consensus
showed broadly the same relations as the Bayesian analysis,
except that the Cape Verdes are resolved as sister to continental
sub-Saharan Africa (AF2) with a BS of 5. The grouping of the
Azores and Madeira (BS . 5) and the Canaries-North Africa
(BS ¼ 4) were well supported.
Taxa unambiguously optimized onto nodes of interest are
listed in Table 2. Under the MP criterion, the inclusion of the
Cape Verde Islands within a sub-Saharan African clade is
supported by 37 synapomorphic presences, nine of which are
endemic. Of these, 11 receive BaSP values under ML .95%.
This clade is also supported by the shared absence of 14 taxa,
of which one has a BaSP value .95% under ML. Within subSaharan Africa, the Cape Verdes are characterized by the
autapomorphic presence of the endemic genus Perssonia and
five other endemic species (Table 5), as well as the homoplastic
presence of 23 species that do not occur elsewhere in subSaharan Africa. Seven of those homoplastic occurences,
namely Neckera intermedia, Plasteurhynchium meridionale,
Philonotis rigida, Ptychomitrium nigrescens, Rhynchostegium
megapolitanum, Tortula solmsii, and Trichostomum contortum,
are shared with the EurAsAf clade. Cryptoleptodon longisetus
is the only species that could be considered a Macaronesian
element in the Cape Verde flora as this species has a
homoplastic distribution spanning the Cape Verdes, Madeira,
and the Canaries.
No less than 93 synapomorphic presences, 22 of which are
endemic to the EurAsAf clade, characterize the inclusion of
Macaronesia s.s. within the EurAsAf clade. Forty-five of the
transitions from absent to present are also supported under ML
by BaSP values .95%. The shared absences of three species
also support this clade although the ‘‘absent’’ state at the
EurAsAf internal node is supported in each case by BaSP
values ,95%.
Within the EurAsAf clade, a subclade comprising western
Asia, North Africa, and the Canaries, is characterized by the
synapomorphic occurrence of the mostly pantropical Gymnostomiella vernicosa, albeit with a BaSP value ,95%, and the
absence of 30 species, for which state ‘‘absent’’ is supported
under ML by BaSp values ,95%. The strong similarities of the
North African and Canarian floras are further emphasized by
the synapomorphic presence of Fissidens sublimbatus and by
the shared absence of 22 additional species (BaSP , 95% in all
cases). Within the Canarian-North African-western Asian
clade, the Canaries are characterized by the autapomorphic
presence of nine endemic species (Table 5) and the
homoplastic occurrence of 17 species that have not been
reported elsewhere within this clade. Among those species,
noteworthy range disjunctions include Tortula bogosica, a subSaharan element; Acaulon fontiquerianum, Fissidens polyphyllus, Gonomitrium seroi, and Isothecium algarvicum, that
are otherwise distributed in Europe; and Amphidium tortuosum,
Echinodium spinosum, Funaria fritzei, Pelekium atlanticum,
and Rhynchostegiella macilenta, that are shared with Madeira.
Madeira and the Azores form a clade with Europe that is, in
turn, sister to the clade formed by western Asia, North Africa,
and the Canaries. The grouping of Madeira, the Azores, and
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TABLE 2. Synapomorphic moss species gains and losses of Macaronesian archipelagos and nesting clades. All reconstructions are based on a maximum
parsimony (MP) optimization onto the strict consensus of the MP analysis. Asterisks indicate that the reconstruction was significant under maximum
likelihood (ML) in .95% of the trees from the Bayesian sample. Endemic synapomorphic transitions are in boldface.
Clade
EurAsAf
MadeiraþAzoresþEUR
MadeiraþAzores
CanariesþAS5þ AF1
CanariesþAF1
Cape Verdesþsub-Saharan Africa
(AF3 and/or AF2 and/or AF4)
Synapomorphies
Losses: Barbula indica, Philonotis uncinata, Syntrichia amphidiacea.
Gains: Acaulon triquetrum, Aloina brevirostris, Anacolia webbii, Braunia alopecura, Bryum donianum*, B. funckii, B.
mildeanum*, B. rubens, B. sauteri, Campylopus brevipilus, Campylostelium pitardii, C. strictum, Cheilothela
chloropus*, Cinclidotus fontinaloides*, Cirriphyllum crassinervium*, Crossidium geheebii*, Cryphaea heteromalla,
Cyclodictyon laetevirens, Cynodontium bruntonii, Dialytrichia mucronata*, Dicranella howei*, Encalypta streptocarpa,
Entosthodon durieui, E. fascicularis, E. obtusus, E. schimperi, Eurhynchium striatum*, Fissidens crassipes, F.
curvatus*, F. ovatifolius, F. rivularis*, F. serrulatus*, Funariella curviseta*, Gigaspermum mouretii, Grimmia crinita,
G. decipiens*, G. nutans, G. tergestina, Gymnostomum viridulum*, Habrodon perpusillus*, Homalia lusitanica*, H.
webbiana*, Homalothecium aureum*, Hyocomium armoricum*, Hypnum cupressiforme var. resupinatum, H.
jutlandicum*, Leptobarbula berica*, Leptodon smithii, Leucobryum glaucum, Mnium hornum, Neckera complanata,
Neckera crispa*, N. pumila, Orthtrichum patens, Oxyrrhynchium pumilum*, O. schleicheri*, O. speciosum*,
Palustriella commutata, Philonotis rigida*, Plagiomnium affine*, P. undulatum*, Plasteurhynchium meridionale*, P.
striatulum, Pogonatum aloides*, P. nanum*, Pottia viridifolia, Rhabdoweisia fugax, Rhynchostegiella curviseta*, R.
durieui, R. teneriffae*, R. tenella*, Rhynchostegium confertum*, R. megapolitanum*, Scorpiurium circinatum*, S.
deflexifolium, Sematophyllum substrumlosum, Sphagnum subnitens, Thamnobryum alopecurum*, T. maderense,
Timmiella barbuloides*, Tortella inflexa, T. nitida*, Tortula canescens*, T. cuneifolia*, T. marginata*, T. pallida, T.
revolvens, T. solmsii*, T. vahliana, Trichostomum triumphans, Weissia condensa, W. longifolia, Zygodon forsteri.
Gains: Andreaea heinemannii, Campylopus shawii, Fissidens polyphyllus, Glyphomitium daviesii, Grimmia arenaria,
Hypnum uncinulatum, Isothecium algarvicum, Myurium hochstetteri, Neckera intermedia, Pseudotaxiphyllum
laetevirens*, Ptychomitrium nigrescens, P. polyphyllum, Rhampidium purpuratum, Tetrastichium fontanum, T. virescens,
Ulota calvescens.
Losses: Acaulon muticum, Aloina brevirostris, Amphidium lapponicum, Anomodon viticulosus, Aulacomium androgynum,
Bryum cellulare, B. funckii , B. gemmiferum, B. gemmilucens, B. pallens, B. pallescens, Campylostelium pitardii,
Crossidium aberrans, C. squamiferum, Didymodon australasiae, Ditrichum pusillum, Encalypta streptocarpa,
Entosthodon durieui, E. facicularis, E. schimperi, Fissidens exilis, Gigaspermum mouretii, Grimmia anodon, G. crinita,
G. nutans, G. tergestina, Hyophila involuta, Lescuraea mutabilis, Neckera menziesii, N. pennata, Orthotrichum
acuminatum, O. patens, O. pumilum, O. striatum, Philonotis caespitosa, Plasteurhynchium striatulum, Pleuridium
subulatum, Pohlia andalusica, P. cruda, P. wahlenbergii, Pottia viridifolia, Protobryum bryoides, Pterygoneuron
subsessile, Pylaisia polyantha, Pyramidula tetragona, Racomitrium ellipticum, Sanionia uncinata, Schistidium flaccidum,
Scleropodium cespitans, Sphagnum affine, S. palustre, S. papillosum, S. pylaesii, Syntrichia fragilis, S. montana, S.
papillosa, S. virescens, Thuidium delictatulum, Timiella anomala, T. flexiseta, Tortella fragilis, T. inflexa, Tortula
bolanderi, T. pallida, Trichodon cylindricus, Trichostomum tenuirostris, Weissia condensa, W. longifolia.
Gains: Alophosia azorica, Andoa berthelotiana, Brachymenium notarisii, Campylopus incrassatus, Daltonia stenophylla,
Echinodium prolixum, Fissidens coacervatus, F. luisieri, F. sublinaefolius, Leucodon canariensis, Neckera
cephalonica, Philonotis hastata.
Gains: Gymnostomiella vernicosa.
Losses: Andreaea alpestris, A. rothii, Bryoerythrophyllum inaequifolium, Bryum gemmiferum, B. tenuisetum, Campylopus
brevipilus, Cyclodictyon laetevirens, Dicranella schreberiana, Dicranum scottianum, Fissidens asplenioides, F. bryoides
var. caespitans, Grimmia ramondii, G. torquata, Hyophila involuta, Isopterygium tenerum, Kiaeria blyttii, Leucobryum
albidum, Orthodontium pellucens, Pohlia proligera, Racomitrium fasciculare, Rhabdoweisia fugax, Rhytidiadelphus
loreus, Sphagnum affine, S. magellanicum, S. papillosum, S. pylaesii, S. rubellum, Splachnobryum obtusum, Timmiella
flexiseta, Zygodon forsteri.
Gains: Fissidens sublimbatus.
Losses: Andreaea rupestris, Atrichum tenellum, Blindia acuta, Brachythecium mildeanum, Bryoerythrophyllum
ferruginascens, Bryum subapiculatum, Campylopus subulatus, Dicranella rufescens, Dicranum majus, Diphyscium
foliosum, Hygrohypnum luridum, Hypnum cupressiforme var. resupinatum, Paraleucobryum longifolium, Orthodontium
gracile, Pohlia bulbifera, P. longicolla, Racomitrium elongatum, Rhytidiadelphus squarrosus, R. subpinnatus, Sphagnum
girgensohnii, S. squarrosum, Thuidium delictatulum.
Losses: Amblystegium serpens, Fissidens bryoides*, F. taxifolius, Hymenostylium recurvirostrum, Orthotrichum rupestre,
Pohlia cruda, P. nutans, P. wahlenbergii, Sanionia uncinata, Sphagnum magellanicum, Syntrichia laevipila, S.
papillosa, Tortella fragilis, Tortula atrovirens.
Gains: Barbula bolleana*, Brachymenium acuminatum, B. exile*, B. notarisii, B. philonotula, Bryoerythrophyllum
campylocarpum*, Bryum apiculatum, B. cellulare, Campylopus flaccidus, Crossidium squamiferum, Cyclodictyon
laetevirens, Didymodon maschalogena, D. rigidulus, Ditrichum pallidum, Fabronia leikipiae, Fissidens androgynus*,
F. bogosicus*, F. sciophyllus*, F. usambaricus, Groutiella laxotorquata, Gymnostomiella vernicosa, Herpentineuron
toccoae*, Leptodon smithii, Leptophascum leptophyllum, Grimmia laevigata, Hedwigia ciliata s.l., Palamocladium
leskeoides*, Pleuridium acuminatum, Pseudephemerum nitidum, Pseudoleskea pseudoattenuata*, Pterogonium gracile*,
Ptychomitrium subcrispatum*, Splachnobryum obtusum, Syntrichia amphidiacea, Tortula bogosica, Trichostomum
crispulum, T. tenuirostris.
Europe is characterized by 16 synapomorphic species presences (15 BaSP , 95%), four of which are endemic. Within this
clade, the Madeira þ Azores grouping is supported by 12
synapomorphic species, four of which are strictly endemic. The
non-endemic transitions, supported under ML by BaSP values
all ,95%, represent disjunct distributions patterns: Andoa
berthelotiana, Fissidens coacervatus, Leucodon canariensis,
and Neckera cephalonica are shared with the Canaries;
Daltonia stenophylla with tropical America; Brachymenium
notarisii and Campylopus incrassatus with sub-Saharan Africa;
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TABLE 3. Synapomorphic liverwort species gains and losses of Macaronesian archipelagos and nesting clades. All reconstructions are based on maximum
parsimony (MP) optimization onto the 50% majority-rule consensus of the Bayesian sample of trees. Asterisks indicate that the reconstruction was
significant under maximum likelihood (ML) in .95% of the trees from the Bayesian sample. Endemic synapomorphic transitions are in boldface.
Clade
Synapomorphies
EurAsAf and EuropeþAF1þMadeiraþ
CanariesþAzores
Gains: Asterella africana, Athalamya spathysii, Cephaloziella baumgartneri*, C. calyculata, Exormotheca
pustulosa*, Fossombronia angulosa*, F. caespitiformis, F. echinata, F. husnotii*, Frullania tamarisci*, F.
teneriffae, Gongylanthus ericetorum, Jubula hutchinsiae, Lejeunea eckloniana*, Lophocolea fragrans*, Lophozia
turbinata, Mannia androgyna, Porella arboris-vitae, P. canariensis, Riccia bicarinata, R. ciliata, R. ciliifera*, R.
huebeneriana, R. ligula, R. papillosa, R. subbifurca, R. trabutiana, R. warnstorfii, Riella cossoniana, Scapania
gracilis, Southbya nigrella, S. tophacea*.
Losses: Cephalozia catenulata, Cladopodiella francisci, Herbertus sendtneri, Hygrobiella laxifolia, Marsupella
sprucei, Metzgeria leptoneura, M. temperata, Plagiochila exigua.
Gains: Acrobolbus wilsonii*, Adelanthus decipiens*, Aphanolejeunea microscopica*, Cephalozia catenulata, C.
crassifolia*, Cephaloziella dentata*, Cladopodiella francisci*, Cololejeunea minutissima*, Colura calyptrifolia,
Drepanolejeunea hamatifolia*, Frullania azorica*, F. microphylla*, Harpalejeunea molleri*, Herbertus
sendtneri, Hygrobiella laxifolia*, Kurzia pauciflora*, Lejeunea flava*, L. hibernica*, L. lamacerina*, L.
mandonii, Lepidozia cupressina*, L. pearsonii, Leptoscyphus cuneifolius*, Marchesinia mackai*, Marsupella
adusta*, M. profunda*, M. sparsifolia, M. sprucei, Metzgeria fruticulosa, M. leptoneura*, M. temperata,
Plagiochila bifaria*, P. exigua, P. punctata*, P. spinulosa, Radula aquilegia*, R. carringtonii*, R. holtii*, Riccia
beyrichiana, Saccogyna viticulosa*, Telaranea europaea*.
Losses: Athalamya spathysii*, Frullania ericoides*.
Gains: Acanthocoleus aberrans, Aphanolejeunea azorica, A. sintenesii, Heteroscyphus denticulatus, Jungermannia
callithrix, Odontoschisma prostratum, Plagiochila retrorsa, Radula nudicaulis, R. wichurae.
Losses: Porella arboris-vitae, Riccia atromarginata, R. frostii, Riella affinis, R. cossoniana, Southbya nigrella,
Sphaerocarpos michelii.
Gains: Cololejeunea schaefferi, Frullania polysticta, Lejeunea canariensis, Plagiochila stricta, P. virginica,
Radula jonesii.
Losses: Anastrophyllum minutum, Barbilophozia attenuata, Blepharostoma trichophyllum, Calypogeia integristipula,
C. neesiana, Fossombronia wondraczekii, Herbertus sendtneri, Lepidozia pearsonii, Lophozia excisa, L. incisa, L.
longiflora, L. turbinata, L. ventricosa, Marsupella sparsifolia, M. sphacelata, Riccia beyrichiana, R. huebeneriana,
Scapania scandica, Trichocolea tomentella.
Gains: Acrolejeunea emergens, Cololejeunea minutissima, Cyatodium cavernarum, Exormotheca pustulosa,
Frullania socotrana, F. spongiosa*, Lejeunea caespitosa*, L. eckloniana, L. flava, Marchantia paleacea, M.
pappeana*, Plagiochasma eximium*.
EuropeþMadeiraþCanariesþAzores
MadeiraþCanariesþAzores
MadeiraþCanaries
Cape Verdesþsub-Saharan Africa
and Philonotis hastata is a widespread tropical species.
Support for the Madeira þ Azores grouping is also provided
by the synapomorphic absence of 68 species from the
archipelagos (BaSP values ,95%).
The Madeiran flora is characterized by the endemic genus
Nobregaea, eight endemic species, and one endemic variety
(Table 5), as well as the homoplastic occurrence of species
elesewhere absent in the (Europe þ Azores þ Madeira) clade.
These include five species shared with the Canaries (discussed
earlier), the sub-Saharan Brachymenium philonotula, the
neotropical Syntrichia bogotensis, and several species, namely
Dicranella campylophylla, Ditrichum difficile, and D. punctulatum, whose distributions span several continents.
The Azores are characterized by the autapomorphic presence
of six endemic species (Table 5) and the homoplastic
TABLE 4. Autapomorphic, endemic pteridophyte taxa of each Macaronesian archipelago.
Archipelago
Cape Verde
Azores
Madeira
Canaries
Endemics
—
Polypodium macaronesicum subsp. azoricum, Asplenium
aethiopicum subsp. nov.?, Dryopteris azorica, D.
crispifolia, Isoetes azorica, Marsilea azorica.
Hymenophyllum maderense, Arachniodes webbianum subsp.
webbianum, Dryopteris aitoniana, D. maderensis,
Polystichum drepanum, P. falcinellum.
Cheilanthes pulchella, Asplenium filare subsp. canariense, A.
octoploideum, Dryopteris oligodonta.
occurrence of the sub-Saharan Campylopus flaccidus and
Tortula bogosica, the neotropical Campylopus cygnaeus, and
two species, Fissidens serratus and Philonotis uncinata, with
less specific distributions that span several continents.
Liverworts—The liverwort data matrix (Appendix S1 and
S3; see Supplemental Data accompanying online version of
this article) comprises 217 taxa. As with both pteridophyte and
moss analyses, Macaronesia s.l. is not resolved as a clade in the
50% majority-rule consensus of the 1364 trees sampled during
the Bayesian procedure (Fig. 4). The Cape Verdes are sister to
the three regions of sub-Saharan Africa (AF2–AF4; posterior
probability ¼ 100%) whereas the Canaries, Azores, and
Madeira are again included within the EurAsAf clade (posterior
probability ¼ 100%). Constraining the Markov chains to only
sample trees that fit with a monophyletic Macaronesian
concept resulted in topologies that displayed significantly
lower ln L values (P , 0.001), and a monophyletic
Macaronesia s.l. concept is thus rejected.
Within the EurAsAf clade, a monophyletic Macaronesia s.s.
is resolved and supported by a posterior probability of 72%.
Within this clade, the Canaries and Madeira form a
monophyletic group with a 95% posterior probability.
Macaronesia s.s. is sister to Europe, a relationship that is well
supported (posterior probability ¼ 99%).
The single most parsimonious tree of length 685 steps (CI ¼
0.317; RI ¼ 0.623) resulting from the analyses of the 207
informative characters suggests at first sight a somewhat different
scenario (data not shown). The Cape Verdes are again included
within a sub-Saharan clade (BS¼ 5) and as sister area to AF2 (BS
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Fig. 3. Phytogeographic affinities of the Macaronesian moss flora
inferred from a 50% majority-rule consensus of 1279 trees sampled after
convergence of three independent Markov chains implementing a model
of equal transition rates. See Fig. 2 for definitions of abbreviations.
Fig. 4. Phytogeographic affinities of the Macaronesian liverwort flora
inferred from a 50% majority-rule consensus of 1364 trees sampled after
convergence of three independent Markov chains implementing a model
of equal transition rates. See Fig. 2 for definitions of abbreviations.
¼ 5), while the three other archipelagos are included within the
EurAsAf clade. Within the latter, however, the Azores þ Madeira
(BS ¼ 1) form a clade that is sister to Europe (BS ¼ 3), while the
Canary Islands are resolved as sister to northern Africa (BS ¼ 1).
Within a parsimony framework, constraining Macaronesia
s.s. to monophyly resulted in a topology only three steps longer
than the optimal topology. The value of p/2 of the associated
KH test was 0.36, suggesting that the data do not significantly
support the rejection of a monophyletic Macaronesia s.s. Given
that the results from the Bayesian analysis are consistent with a
monophyletic interpretation of Macaronesia s.s. and because
Macaronesia s.s. cannot be significantly rejected based upon
the MP analyses, the optimal MP topology, wherein the
Canaries, the Azores, and Madeira appear in different (and
weakly supported) clades, was not used to investigate species
optimizations. Rather, these were investigated on the 50%
majority-rule consensus tree from the Bayesian sample.
The inclusion of the Cape Verdes within sub-Saharan Africa
is supported by the synapomorphic presence of 12 species, six
of which are endemic (Table 3). The Cape Verdes lack any
endemic species but are characterized by the presence of
Fossombronia angulosa, Frullania tamarisci, Lejeunea lamacerina, and Marchesinia mackai, which do not occur anywhere
else in sub-Saharan Africa and are shared with the EurAsAf
clade.
The inclusion of the Azores, Madeira, and the Canaries
within the EurAsAf clade is supported by 32 synapomorphic
TABLE 5. Autapomorphic, endemic moss taxa of each Macaronesian
archipelago. Endemic genera are in boldface.
Archipelago
Endemics
Cape Verde
Bryum anomodon, Entodon pseudoseductrix, Fissidens
allorgei, Funaria chevalieri, Perssonia sanguinea,
Pseudoleskea bollei.
Breutelia azorica, Echinodium renauldii, Fissidens azoricus,
Sphagnum nitidulum, Thamnobryum rudolphianum,
Trematodon perssonorum.
Brachythecium percurrens, Bryoxyphium madeirense,
Echinodium setigerum, Fissidens microstictus, F.
nobreganus, Nobregaea latinervis, Plagiomnium undulatum
var. madeirense, Pohlia luisieri, P. maderensis,
Thamnobryum fernandesii.
Aloina humilis, Entosthodon krausei, Grimmia curviseta,
Orthotrichum handiense, Platyhypnidium torrenticola,
Rhynchostegiella bourgeana, R. trichophylla, Tortella
limbata, Tortula ampliretis.
Azores
Madeira
Canaries
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TABLE 6. Autapomorphic, endemic liverwort taxa of each Macaronesian
archipelago.
Archipelago
Endemics
Cape Verde
Azores
—
Bazzania azorica, Cheilolejeunea cedercreutzii, Leptoscyphus
azoricus, Tylimanthus azoricus.
Frullania sergiae, Plagiochila maderensis, Porella inaequalis,
Riccia atlantica, Tylimanthus madeirensis.
Riccia teneriffae.
Madeira
Canaries
species presences, nine of which are well supported with high
(.95%) BaSP values, and nine of which are endemic, and by
the absence of a further eight species (Table 3). Within the
EurAsAf clade, the sister group relationship between Macaronesia s.s. and Europe is supported by 41 synapomorphic
presences, 29 of which have BaSP values .95% and 10 of
which are endemic, and two are synapomorphic losses.
Macaronesia s.s. is characterized by two endemic species
whose distribution spans across all archipelagos, namely,
Heteroscyphus denticulatus and Radula wichurae, and seven
disjunctly distributed taxa that occur nowhere else within the
EurAsAf clade and are of neotropical (Aphanolejeunea
azorica, A. sintenesii, Jungermannia callithrix, Odontoschisma
prostratum, Plagiochila retrorsa and Radula nudicaulis) and
pantropical (Acanthocoleus aberrans) origin (Table 6). A
monophyletic interpretation of Macaronesia s.s. is further
supported by the synapomorphic absence of seven species, all
of which, however, have BaSP values of ,95%. Within
Macaronesia s.s., the Azores are characterized by four endemic
species (Table 6) and the homoplastic occurrence of Jamesionella rubricaulis, Plagiochila longispina, P. papillifolia, (all
predominantly neotropical), and the sub-Saharan Lepidozia
stuhlmannii. The sister-group relationship between the Canaries and Madeira is supported by the endemics Cololejeunea
schaefferi, Frullania polysticta, Lejeunea canariensis, and
Radula jonesii, all of which have BaSp values ,95%. A suite
of 19 synapomorphic absences, albeit with low support under
ML (Table 6), further characterizes this clade. In addition, the
New World species Plagiochila stricta and P. virginica are
shared by the Canaries and Madeira, but occur nowhere else
whithin EurAsAf. Their presence at the internal node joining
the two archipelagos is, however, supported by low BaSP
values ,95%.
Within the Madeiran-Canarian clade, Madeira is characterized by a suite of five endemic species (Table 6) and the
homoplastic presence of the Neotropical Cephaloziella granatensis. The Canaries possess one endemic, Riccia teneriffae,
and are further characterized by the homoplastic presence of
the sub-Saharan Frullania obscurifolia.
DISCUSSION
Relationships of the Cape Verde cryptogamic flora—The
results presented in this paper suggest that the Macaronesian
region, comprising the Cape Verdes together with the Azores,
Madeira, and Canaries, does not represent a natural floristic
unit for bryophyte and pteridophyte groups when all native
taxa are included. All three analyses are therefore consistent
with the view of Lobin (1982) that the flora of the Cape Verdes
is more closely related to the flora of sub-Saharan Africa than
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to the other Macaronesian archipelagos. The well-supported
Cape Verde-tropical African sister group relationship for each
cryptogamic group and the non-monophyly of the Macaronesian region challenge the Engler refugium model to explain the
origin of the Macaronesian flora s.l. The large number of taxa
shared by the Cape Verdes and the near-continent rather
suggests that the dynamic interchange model best explains the
present day flora of the Cape Verdes.
Among the bryophytes distributed on the Cape Verdes,
Cryptoleptodon longisetus is the only species that could be
considered a ‘‘Macaronesian element.’’ The distribution of this
species spans three of the four archipelagos, namely, the Cape
Verdes, Canaries, and Madeira, and its occurrence in moist,
protected habitats in natural forests (Hedenäs, 1992) may
indeed indicate a relictual origin for this species. Among
pteridophytes, four taxa have a homoplastic, but exclusively
Macaronesian distribution, that encompasses the Cape Verdes
and other Macaronesian archipelagos. Notholeana marantae
subsp. subcordata and another somewhat xerophytic rock fern,
the dodecaploid Asplenium aethiopicum subsp. braithwaitii (a
local variant of a widely distributed polyploid complex with its
center of diversity in southern Africa), are both exclusively
distributed in Madeira, the Canaries, and Cape Verdes. The
claim of these taxa to be relictual is perhaps weakened by their
high ploidy level (Vogel et al., 1999) and their restriction to
xerophytic habitats. Dryopteris oligodonta, however, is
thought to have its closest relatives in Madagascar (Lobin et
al., 1998) and is unique to the Cape Verdes and Canaries,
where it is abundant in humid laurisilva habitats in the latter.
The distribution of this species may be relictual in nature. The
fourth fern species within the homoplastic floristic element
common to the Cape Verdes and Madeira-Canaries is
Adiantum reniforme s.l. This species complex is also present
in tropical East Africa. Such a disjunct distribution would also
be consistent with the Engler refugium model. However,
although inseparable by gross morphology, the Canarian and
Madeiran plants are cytologically distinct (Manton et al.,
1986), the former tetraploid, the latter decaploid. Unfortunately, the cytology of the disjunct Cape Verdean, African,
Mascarene and Asian examples, which have collectively been
referred to A. reniforme s.l., is unknown. The possible relictual
status of the Macaronesian taxa will thus remain uncertain until
their origin and relationships are established.
Relationships of the Azores, Madeira, and Canary Islands
floras—All three analyses resolve the Azores, Madeira, and the
Canary Islands in a clade with Europe, North Africa, and
southwest Asia.
The moss and pteridophyte data sets are also consistent in
resolving Madeira and the Azores as sister areas, a clade that is
supported by four and four endemic synapomorphies, the
synapomorphic presence of a further four and eight nonendemic species, and the synapomorphic absence of eight and
68 species in the pteridophyte and moss analyses, respectively.
The dynamic interchange model offers a possible explanation for the shared absence of taxa from the Azores and
Madeira. In some instances, absences may reflect the stochastic
nature of the interchange between continental and island areas
with the incomplete colonization of the islands from continental source areas. In others, this pattern probably reflects the lack
of suitable niches on the archipelagos. For example, a
conspicuous calcicolous element comprising the mosses
Acaulon muticum, Aloina brevirostris, Amphidium lapponi-
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V ANDERPOORTEN
ET AL .—D OES
cum, Anomodon viticulosus, Crossidium aberrans, C. squamiferum, Encalypta streptocarpa, Entosthodon fascicularis,
Grimmia crinita, G. tergestina, Lescuraea mutabilis, Neckera
menziesii, N. pennata, Plasteurhynchium striatulum, Protobryum bryoides, Pterygoneuron subsessile, Tortella inflexa,
Weissia condensa, and W. longifolia is absent from the Azores
and Madeira.
While the four pteridophyte and four moss species that are
endemic to the Azores-Madeira clade could be considered
evidence for the presence of traces of Tertiary relictualism in
the cryptogamic flora, there is at least some evidence to suggest
that these taxa are more likely to have evolved in situ by
isolation following long-distance dispersal from the New
World. Among the endemic pteridophytes, Huperzia dentata
is the only Old World representative of the otherwise
exclusively New World section Reflexa. As a hexaploid (I.
Manton [deceased], unpublished data), this species is likely to
be a derived representative of this distinct lineage and not basal
to it. Colonization of Macaronesia from the new World best
explains the observed distribution and known relationships of
this taxon. The relationships of Diphasiastrum madeirense
remain to be resolved, but some aspects of its growth form
suggest closer affinities to the North American D. digitatum
than to Eurasian taxa. Elaphoglossum semicylindricum,
described from Madeira, was regarded as conspecific with
material from Jamaica (Proctor, 1985). Proctor (1985, p. 506),
however, noted that ‘‘members of this complex also occur in
South America and through the paleotropics, but they may be
recognizable as distinct species.’’ In Davidse et al. (1995), it is
clear that several distinct entities have been treated under E.
paleaceum, a synonym of E. semicylindricum. Further work is
clearly needed to establish whether the Macaronesian material
is distinct, but its affinities to the New World are incontrovertible. A further New World link is provided by the Azorean
endemic aquatic Isoetes azorica, which has been shown to be
most closely related to the North American I. tuckermannii
(Britton and Brunton, 1996).
Among bryophytes, the very limited molecular phylogenetic
evidence for the origin of Macaronesian endemics suggests that
the liverworts Leptoscyphus azoricus and Plagiochila maderensis are of recent neotropical origin (Rycroft et al., 2004;
Vanderpoorten and Long, 2006). Other Macaronesian endemic
liverworts, such as Tylimanthus azoricus, are also suspected to
be of recent neotropical origin (Schumacker, 2001).
In addition to a New World link for the endemic taxa
supporting the Azores þ Madeira clade, there is also a
substantial New World element in the non-endemic pteridophyte and moss flora of the archipelagos that supports this
grouping. The pteridophytes Ceradenia jungermannioides and
Grammitis marginella are disjunct in the Azores and Madeira
but have their main distribution area on the American
continent. Similarly, five of the nine species of the moss
genus Campylopus present in the Azores have a distribution
range that spans Macaronesia and the Caribbean islands
(Frahm, 1999). In the liverwort genus Plagiochila, more than
50% of the species found on Madeira also occur in the
neotropics (Sim-Sim et al., 2005). A complete extinction of all
these taxa from Europe, western Asia, and northern Africa
during the Ice Ages cannot be completely ruled out. Indeed,
such an explanation may be necessary for the moss genus
Echinodium, which is currently restricted to the Macaronesian
archipelagos within the EurAsAf clade, but is known from
European Eocene fossils (Frahm, 2004). However, the
M ACARONESIA
EXIST ?
635
predominant pattern evident from both bryophyte and pteridophyte analyses is consistent with the view that the Madeiran
and Azorean archipelagos have served as stepping stones for
the eastward spread (and occasional isolation in the case of
endemics) of American taxa (Sim-Sim et al., 2005). Muñoz et
al. (2004) demonstrated that wind connectivity rather than
geographic proximity is the main force driving current
bryophyte distributions. Frequent depressions moving rapidly
eastward at relatively low altitude (3000 m) from the American
coasts and tropical cyclones of west Caribbean origin that can
carry even large propagules may have provided a mechanism
for colonization of these archipelagos from the New World
(Schäfer, 2003).
In the liverwort and pteridophyte ML analyses, Macaronesia
s.s. is resolved as a monophyletic group that is sister to Europe
in the 50% majority-rule consensus of the trees sampled during
the Baysian procedure. This relationship is also recovered in
50% of MP trees from the parsimony analysis of the
pteridophyte data. In liverworts, MP recovers a different set
of relationships. However, a monophyletic Macaronesia s.s. is
only three steps longer and under the MP criterion cannot be
rejected.
Macaronesia s.s. corresponds to the circumscription of the
region first proposed by Engler (1879) and before subsequent
authors expanded the concept to include the Cape Verdes (e.g.,
Dansereau, 1961; Takhtajan, 1969; Bramwell, 1972, 1976)
and, in some cases, continental enclave areas (Sunding, 1979).
The recognition of Macaronesia s.s. is in marked contrast to
more recent classifications that have not recognized a
Macaronesian s.s. region (e.g., Lobin, 1982; Rivas-Martinez
et al., 2004).
The sister-group relationship between Macaronesia s.s. and
Europe is supported by an Atlantic fringe element, i.e., a suite
of taxa that occur only on the three archipelagos and the
western seaboard of Europe. These taxa include the ferns
Ophioglossum azoricum, Hymenophyllum tunbrigense (also
distributed in the Americas and southwestern Asia), and H.
wilsonii, rarely with disjunct refugia elsewhere in the case of
Dryopteris aemula and Trichomanes speciosum and the
liverworts Acrobolbus wilsonii, Adelanthus decipiens, Aphanolejeunea microscopica, Cololejeunea minutissima, Colura
calyptrifolia, Drepanolejeunea hamatifolia, Frullania azorica,
F. microphylla, Harpalejeunea molleri, Herbertus sendtneri,
Hygrobiella laxifolia, Lejeunea flava, L. hibernica, L.
lamacerina, L. mandonii, Lepidozia cupressina, L. pearsonii,
Leptoscyphus cuneifolius, Marchesinia mackai, Marsupella
adusta, M. profunda, M. sparsifolia, M. sprucei, Metzgeria
fruticulosa, M. leptoneura, M. temperata, Plagiochila bifaria,
P. exigua, P. punctata, P. spinulosa, Radula aquilegia, R.
carringtonii, R. holtii, Saccogyna viticulosa, and Telaranea
europaea. This suite of hyper-Atlantic taxa has, at least in
ferns, long been regarded as relictual of a broader Tertiary
distribution range currently restricted, as in H. tunbrigense, to
disjunct sheltered sandstone gorges refugia of Central Europe,
eastward through northern Turkey and into the former USSR
(Drude, 1902; Klein, 1926; Richards and Evans, 1972). The
distributions of two further species that are widespread in
Macaronesia and also occur in Macaronesian enclave areas on
the nearby continent, also support the refugium hypothesis:
Diplazium caudatum, which occurs throughout Macaronesia
and is known from the Sierras just north of Algeciras in
southernmost Spain, and Asplenium hemionitis, which similarly occurs on all Macaronesian archipelagos and in several
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coastal enclave areas in North Africa and Portugal. In addition,
a record of Asplenium aethiopicum from the Moroccan AntiAtlas enclave, an area that also harbors Dracaena draco
(Benabid and Cuzin, 1997), may prove to be of the insular
subsp. braithwaitii, and Polypodium macaronesicum s.l. has
been reported from the southern Spanish Macaronesian enclave
north of Algeciras (Greuter et al., 1984), although this record
needs confirmation. Both distributions would similarly be
consistent with a broadly interpreted Engler refugium model
linking the Azores-Madeiran-Canarian pteridophyte flora with
that of putative continental enclave areas.
Asplenium anceps is endemic to the three northern
archipelagos and would also support the resolution of these
three areas as a clade. Whereas this species is only known from
a single collection (Lovis et al., 1977) in the Azores, it is
implicated in the parentage of the Azorean endemic A.
azoricum and its Iberian-North African counterpart A.
trichomanes subsp. coriaceifolium (¼ A. azomanes), neither
of which is currently sympatric (Rumsey et al., 2004). The role
of A. anceps in the parentage of these taxa suggests that this
species might once have been both more abundant on the
Azores and, conceivably, present in the nearby continent. If
this is the case, then the current distribution of this species
would represent a contraction of its historical distribution, a
scenario consistent with the Engler refugium model.
Selaginella kraussiana (otherwise confined to tropical and
southern Africa) and Asplenium monanthes (a pantropical
species), which both represent a tropical element with a
northern extension into the region, also support a northern
archipelago grouping, as do the Madeiran-Canarian endemics
Asplenium lolegnamense and Polypodium macaronesicum
subsp. macaronesicum.
In addition, the interpretation of the speciation in Dryopteris
guanchica, currently restricted to the Canaries and along the
Atlantic coast of Iberia, suggests a link between Madeira and
the Canaries/Europe that is not evident from extant distribution
data alone. Dryopteris guanchica is a polyploid derivative of a
cross involving D. maderensis, a species endemic to Madeira,
and D. aemula, a species present on all three northern
Macaronesian archipelagos but otherwise distributed along
the Atlantic coasts of Europe and in Turkey (Davis et al.,
1988). At present, the parental taxon D. maderensis and its
derivative D. guanchica have mutually exclusive distributions.
However, for one to have arisen from the other, one or both
must have been more widespread in the past. Indeed, a range of
dispersal–extinction scenarios could explain the origins of D.
guanchica and the extant distributions of these two taxa: (1)
Dryopteris guanchica had its origins in Madeira, dispersed to
the Canaries and Europe, and subsequently went extinct from
Madeira, or (2) D. maderensis was more widespread, formerly
occurring in the Canary Islands, where hybridization with D.
aemula gave rise to D. guanchica before D. maderensis
became extinct from the Canaries and D. guanchica dispersed
to Europe; (3) as with scenario (2), but with D. maderensis
present and giving rise to D. guanchica in Europe before going
extinct there and D. guanchica colonizing the Canaries from
Europe; and (4) D. maderensis historically present in both
Europe and Canaries, independently giving rise to D.
guanchica in these two areas and subsequently going extinct
from both. Whatever the scenario involved, the speciation of D.
guanchica requires that the species was present across several
archipelagos and the southwestern coasts of Europe, a pattern
that is again consistent with the Engler refugium model.
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The moss analyses differ from those of the pteridophytes and
liverworts with respect to the placement of the Canaries within
the EurAsAf clade. For mosses, the hypothesis of a common
origin of the flora of Macaronesia s.s. is rejected and the
Canaries are resolved as sister area to North Africa. This
placement lends further support to the dynamic interchange
model by indicating a close relationship with the nearby
continent rather than to a common, relictual Tertiary origin for
the archipelago floras. It is notable that the relationship
between the Canaries, northern Africa, and western Asia, and
the sister group relationship between the Canaries and northern
Africa, are supported by the shared loss of 30 and 22 species,
respectively. A substantial proportion of those species, namely
Andreaea rothii, Blindia acuta, Bryoerythrophyllum ferruginascens, Campylopus brevipilus, C. subulatus, Diphyscium
foliosum, Fissidens bryoides var. caespitans, Hypnum cupressiforme var. resupinatum, Leucobryum albidum, Orthodontium
gracile, Rhytidiadelphus loreus, Sphagnum affine, S. papillosum, and S. pylaesii, are of (sub)oceanic affinities, and this
suggests that the synapomorphic absences characteristic for the
Canaries and northern Africa are at least partly explained by
ecological factors. The possibility that this result is an artifact
due to a severe limitation in current floristic inventories seems
unlikely because, while the flora of North Africa is still
somewhat under-recorded, recent intensive floristic research
has substantially increased our knowledge of the region’s
bryoflora (Ros et al., 1999). It thus appears that the Canarian
and northern African flora has little floristic individuality and
represents the extension of xerophytic bryofloras of the
Mediterranean areas and the Middle East and of a European
temperate flora in the highest mountains (Tan and Pocs, 2000).
Dispersal, relictualism, and the patterns of relationships of
the archipelago floras—The broad congruence observed
between bryophyte and pteridophyte data sets with regards to
the placement of the Cape Verdes serves to emphasize the
remoteness of these islands from the rest of Macaronesia when
contrasted with the distance between the Cape Verdes and the
near continent. With respect to the northern archipelagos, the
relationships suggested by the moss analyses are incongruent
with a Macaronesia s.s. grouping and support the dynamic
interchange model to explain the predominant floristic pattern
observed. Vanderpoorten and Long (2006) recently proposed
that one interpretation of the non-European and North African
origin of Macaronesian endemic bryophytes and pteridophytes,
which sharply contrasts with the origin of the vast majority of
endemic angiosperms (Carine et al., 2004), is the existence of
extensive gene flow between Macaronesian and continental
populations. Endemic speciation resulting from gene-flow
disruption would thus only be possible in the case of discrete
long-distance dispersal events. The results of the moss analyses
presented in this paper are consistent with this hypothesis. The
recent development of microsatellite loci in bryophytes (Van
der Velde et al., 2000; Long et al., 2006) should help to provide
the necessary framework to test hypotheses of an ancient
isolation vs. continuous gene flow between Macaronesian and
continental populations.
In contrast to the mosses, the liverwort and pteridophyte
analyses are consistent with the concept of Macaronesia s.s.
and thus do not refute the Engler refugium model as an
explanatory hypothesis for the relationships of the floras of
these archipelagos. Differences between the mosses on one
April 2007]
V ANDERPOORTEN
ET AL .—D OES
hand and the liverworts and pteridophytes on the other may be
attributable to differences in the biology of these groups.
Although the MP analyses employed in the present study
are, by definition, based on the concept of synapomorphy and
hence favor vicariance over long-distance dispersal as a
possible explanation for the obtained biogeographical patterns
(Bisconti et al., 2001; Santos, 2005), the fact, that the ML
model, which does not minimize the level of homoplasy but
rather maximizes the probability of the data given a model of
species ‘‘gains’’ and ‘‘losses,’’ returns comparable results,
further suggests that the results are not biased by the optimality
criterion used in the different techniques employed. The level
of homoplasy present in the data, summarized by statistics such
as the consistency index (CI), can actually provide a measure
of the importance of long-distance dispersal. The moss data set
displays the most homoplastic distribution patterns (CI ¼
0.297), followed by liverworts (CI ¼ 0.317), and finally
pteridophytes (CI ¼ 0.443), and the higher levels of homoplasy
in the moss data sets may reflect the greater long-distance
dispersal ability of this group necessary for dynamic
interchange with continental areas. Greater dispersability may
involve, as emphasized, that endemic speciation in Macaronesian bryophytes rely on discrete events of long-distance
dispersal rather than exchanges with nearby continents. The
rarity of successful establishment following long-distance
dispersal may also explain why endemic bryophytes are much
less numerous than for the angiosperm flora. Macaronesian
endemic bryophytes indeed represent only 9% of the
archipelago floras. In the Azores, only 2% are strictly endemic
to the archipelago, and this represents the lowest proportion by
comparison with all the other biota (Borges et al., 2005).
However, this picture based on traditional, morphological
species concepts, is in urgent need of revision. The status of
many of the endemic bryophytes is an area of controversy
(Schumacker, 2001; Sjögren, 2001), and few molecular
investigations have been undertaken to test that those
supposedly endemic species are not conspecific with other,
more broadly distributed taxa (Stech et al., 2001; Feldberg et
al., 2004; Rycroft et al., 2004; Stech and Sim-Sim, 2006;
Vanderpoorten and Long, 2006). On the other hand, actual
genetic differentiation of Macaronesian endemics may have
taken place without any morphological signature of the genetic
divergence. Such a phenomenon, called cryptic speciation, has
been increasingly documented in bryophytes (Shaw, 2001;
McDaniel and Shaw, 2003; Feldberg et al., 2004).
A further point to note is that whilst a monophyletic
Macaronesia s.s. for pteridophytes and liverworts is certainly
consistent with the explanation provided by Engler’s refugium
model, the extent to which this grouping is truly explained by
Engler’model remains to be ascertained. Other explanations,
notably recent (postglacial) colonization of putative continental
refugial areas from Macaronesia s.s. (or vice versa) are also
plausible. In angiosperms, while some groups have trans- or
intercontinental sister group disjunctions consistent with
relictualism through large-scale continental extinction, many
other groups have sister-group relationships with taxa distributed in the western Mediterranean, a pattern that may suggest a
relatively recent origin for these groups (Carine et al., 2004).
Furthermore, in the case of several genera, evidence suggests
that the Macaronesian islands have served as a source area for
continental neo-endemics. In Convolvulus, for example, Carine
et al. (2004) demonstrated that C. fernandesii, a species
endemic to Cabo Espichel in Portugal and thought by
M ACARONESIA
EXIST ?
637
Bramwell and Bramwell (2001) to be a relictual paleoendemic,
is actually the result of more recent colonization from the
Macaronesian region, as evidenced by its placement in a
molecular phylogeny of the group and the extremely low levels
of sequence divergence when compared with its close
Macaronesian relatives.
Macaronesian pteridophyte and liverwort distributions that
are consistent with Engler’s refugium model may similarly
reflect a complex mix of relictualism overlaid by more recent
evolution and dispersal. The allohexaploid Asplenium lolegnamense, for example, is distributed in Madeira and the
Canaries, but is sympatric with its putative parental taxa only in
the Canaries (Van den Heede et al., 2004), a situation that may
suggest northward colonization from the Canaries to Madeira
rather than ancient relictualism. Similarly, within the Adiantum
reniforme complex, the extant decaploid Madeiran plant may
have been derived from the tetraploid Canarian taxon. Both
cases suggest that a northward colonization, possibly in
progress, rather than ancient vicariance, may explain current
species distributions.
Extensive molecular research on Macaronesian taxa is
necessary to determine whether or not spatially congruent
distributions consistent with the Engler refugium hypothesis do
indeed share a common causal explanation. The actual level of
knowledge on the taxonomic status and origin of the
cryptogamic endemic flora is, however, far below that achieved
for angiosperms. An important and necessary task remains to
better understand the evolutionary mechanisms underlying the
floristic patterns described in the present paper.
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