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BS 55 501
Towards an understanding of the distribution of
Ilex L. (Aquifoliaceae) on a World-wide scale
PIERRE-ANDRÉ LOIZEAU, GABRIELLE BARRIERA, JEAN-FRANÇOIS MANEN AND
OLIVIER BROENNIMANN
LOIZEAU, P.-A., BARRIERA, G., MANEN, J.-F. & BROENNIMANN, O. 2005. Towards an understanding of
the distribution of Ilex L. (Aquifoliaceae) on a World-wide scale. Biol. Skr. 55: 501-520. ISSN 0366-
3612. ISBN 87-7304-304-4.
Almost 600 species of Ilex L. (Aquifoliaceae) are now recognized and most of them occur in trop-
ical America and eastern Asia. Only c 30 species are known from North America, four species are
found in Europe, a few on Pacific islands, one in northeastern Australia and one in sub-Saharan
Africa. Fossil data shows that this genus previously had a much wider distribution. Fossils have
been found in Alaska and Iceland, western North America and southern South America, Siberia,
New Zealand and southern Australia. Floral morphology of Ilex species is very uniform at an inter-
specific level, whereas leaf morphology often shows great variability at an intra-specific level
resulting in difficulties of discriminating between the different species. We compared recon-
structed phylogenies based on chloroplast and nuclear DNA sequences, and morphological char-
acters from 47 Ilex species. The plastid phylogeny is strongly correlated with the geographic dis-
tribution of extant species. However the plastid and nuclear phylogenies are not congruent. This
may be due to frequent inter-lineage hybridization events, a process which could explain the high
complexity of this family (i.e. at morphological, genetic, geographical distribution levels). We did
not obtain a resolved phylogeny based on morphological characters. A world-wide distribution
modelling map has been computed by an Ecological Niche Factor Analysis (ENFA) based on 826
Ilex occurrences in tropical America and 12 GIS layers describing the environment. The map of
the potential distribution obtained is consistent with the distribution of the genus at present.
However the model has less predictive probability for the northern hemisphere. Data of pollen
fossil records for all Ilex over the world were mapped at world scale at various geological periods.
Analyses of extant and past distributions of the genus, and phylogenetic results integrated with
climatic patterns have been used to tentatively explain the current distribution pattern of Ilex.
Some hypothesis assuming Bering and North Atlantic land bridge connections, Tertiary relict flo-
ras, long distance dispersal or morphological stasis are congruent with the current disjunct dis-
tribution of the family.
Pierre-André Loizeau, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail: pierre-
andre.loizeau@cjb.ville-ge.ch
Gabrielle Barriera, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail:
gabrielle.barriera@cjb.ville-ge.ch
Jean-François Manen, Conservatoire et Jardin botaniques, Chambésy/Genève, Switzerland. E-mail:
jean-francois.manen@cjb.ville-ge.ch
Olivier Broennimann, Université de Lausanne, Institut d’écologie et de géobotanique, Dorigny/Lausanne,
Switzerland. E-mail: olivier.broennimann@ie-bsg.unil.ch
Introduction
Diversity and distribution
Aquifoliaceae, the holly family, was once repre-
sented by four genera: Ilex L., Nemopanthus
Raf., Phelline Labill. and Sphenostemon Baill.
(Cronquist 1981), but today it includes only
the genus Ilex (Judd et al. 1999; Powell et al.
2000; Loizeau et al. in press), which is com-
posed of almost 600 species. Although cos-
mopolitan, it is very unevenly distributed in
terms of the number of species occurring in
each continent. Ilex occurs mostly in the trop-
ics but extends into temperate regions with
oceanic climates up to 63°N (America, Eura-
sia) and down to 35°S (America, Africa). There
are c 300 species in tropical America (Loizeau
1994), c 250 species in south-east Asia, c 30
species from North America, four species in
Europe (including the endemic species of the
Canary Islands, Madeira and Azores), a few
species in Pacific islands, one in northeast Aus-
tralia and one in sub-Saharan Africa. Tropical
America and south-east Asia are the important
centres of species diversity for this genus.
Species of Ilex are found from lowland to mon-
tane forest (disturbed or primary) up to 4000
meters elevation in the Andes and in the
Himalayan region. The family is usually found
in humid habitats (Martin 1977) and is totally
absent from very dry areas.
Systematics
A world-wide treatment of the genus was done
by Loesener (1901, 1908, 1942). Floral mor-
phology of Ilex species is very uniform at a
inter-specific level whereas, leaf morphology
often shows great variability at an intra-specific
level, resulting in difficulties in discriminating
between different species. Ilex is composed of
dioiceous shrubs or trees with simple and alter-
nate leaves, and small, usually 4-5-merous flow-
ers gathered in cymose inflorescences. Species
are mostly recognized on whether they are
deciduous or evergreen, the size and shape of
leaves, complexity of the cymose inflores-
cences, and the number of floral parts. The fol-
lowing large-scale anatomical studies empha-
sise some of the difficulties encountered when
discriminating between different species
within the genus. Baas (1973) published an
extensive treatment on the wood anatomy of
Ilex. He concluded that Ilex species were impos-
sible to separate using wood anatomy alone.
He made the same conclusion based on a study
of leaf anatomy (Baas 1975). Lobreau-Callen
(1975) studied the pollen of more than half
the species included in Loesener’s works
(1901, 1908) and concluded that Ilex species
could not be separated based on pollen charac-
teristics. Loizeau and Spichiger (1992) pro-
posed a classification based on the structures
of the inflorescence in Ilex. They included an
evolutionary character for the first time into
the classification of Ilex.
Ancient and extant pollen
The pollen of Ilex is very characteristic (Martin
1977) and no other known pollen type could
be confused with it (Fig. 1). The closest pollen
grain morphology to Ilex is that of Coprosma
nertera F. Muell. (Rubiaceae), which has other
502 BS 55
Fig. 1. Ilex teratopis pollen grain (photo J.Wuest).
features that readily distinguish it. The other
taxa with a pollen ornamentation resembling
that of Ilex can easily be separated using other
pollen morphological characters. Ilex represen-
tatives produce low amounts of pollen, they are
insect-pollinated and very little pollen is found
in the atmosphere (Hyde 1961; Clot pers.
comm.). Moreover they have a relatively low
pollen dispersal capacity (Behling et al. 1997).
The oldest findings of pollen attributed to Ilex
originate from the Turonian or earliest upper
Cretaceous in Australia, 90 million years ago
(mya) (Martin 1977). But the genus was appar-
ently already cosmopolitan by the late Cre-
taceaous, since pollen grains of Ilex dated at 70-
85 mya have been found in Africa, western
North America, and South America (Lobreau-
Callen 1975; Martin 1977; Muller 1981). How-
ever, few data (pictures) of these very old fossil
pollens of Ilex have been published.
Molecular analyses
The phylogenetic history of the genus based
on DNA analyses has been studied by Cuénoud
(1998), Cuénoud et al. (2000), Setoguchi and
Watanabe (2000), and Manen et al. (2002).
The chloroplast atpB-rbcL spacer has been
sequenced for 116 taxa represented in most
parts of the world (Cuénoud et al. 2000). The
plastid phylogeny showed four major clades
that were poorly supported and lacked any
resolved hierarchy between them (i.e. an
American, two Asian/N. America, and a
Eurasian clade). Manen et al. (2002) compared
a three-gene plastid phylogeny with a two-gene
nuclear phylogeny based on 47 species selected
among the taxa studied by Cuénoud et al.
(2000). They observed an incongruence
between the two phylogenies, which they con-
sidered due to the probable expression of a
strong inter-specific and interlineage
hybridization, making phylogenetic studies
very complex. The same conclusion was made
by Setoguchi and Watanabe (2000) based on
Asian Ilex of the Bonin and Ryukyu Islands.
These two studies both demonstrated natural
inter-specific hybridization in Ilex. In horticul-
ture, inter-specific hybridization is achieved
relatively easily between different species of the
genus (Galle 1997).
Finally, a relative test of the rate of
nucleotide substitution made by Cuénoud et al.
(2000) gave the age of the common ancestor of
the extant species as 50 million years old. This
age is far from the 90 mya indicated by the fos-
sil records. According to these authors this dif-
ference could be explained by extinction of
the basal branches of extant species, which
then do not represent the entire lineage.
Moreover they consider the Eocene (54-36
mya) as an important era for diversification in
this genus.
Two questions that this paper attempts to
clarify are: (1) Can contradictions between the
past and present distribution of Aquifoliaceae
be explained using a comparative analysis of
fossils and the current distribution of Ilex, that
also integrates the different theories involving
the earth’s history (continental drift, migra-
tory pathways, climate fluctuation) from 90
mya? (2) Can a phylogeny of Ilex, based on
morphological characters, improve the under-
standing of the different migration patterns in
the genus?
Materials and methods
Morphological analyses
For the 47 Ilex species from all over the world,
for which plastid and nuclear phylogeny was
available (Manen et al. 2002), morphological
descriptions including vegetative (leaves, ram-
ets, etc.) and sexual (inflorescence, flower and
fruit) characters were made. Descriptions were
based on herbarium specimens from BM, BR,
COL, F, G, K, MBM, NY, P, S, US, and W. When
necessary, the descriptions were supplemented
with information from literature, mostly Loe-
BS 55 503
sener (1901) and Galle (1997) (Appendix 1).
Within the framework of our research on
Neotropical Aquifoliaceae, 126 morphological
characters were chosen to infer phylogenetic
relationships among the 47 species included in
the present study.
A matrix of characters was built up for the 47
representative species (available at the address
of the first author) and was used to generate
morphological trees with PAUP 4.0b3a (Swof-
ford 2000). The trees were arbitrarily rooted
with Ilex canariensis Poir., which is claimed to be
the most basal taxon (Manen et al. 2002), to
compare their topology with the molecular
phylogenetic trees.
The plastid and nuclear trees (Manen et al.
2002) were used to analyse the character
matrix. Consistency indices (CI) of each char-
acter were tabulated using MacClade (Maddi-
son & Maddison 1992).
Distribution modelling
In the classical approach, distribution model-
ling (e.g., GLMs, McCullagh & Nelder 1989;
GAMs, Hastie & Tibshirani 1987) requires both
presence and absence data. The available Ilex
data do not allow us to use this kind of model
because, as is often the case with herbarium
material, the absence of herbarium collections
from a given place may indicate that taxa are
absent or that there are no collections from
that region. To overcome this problem of
absence data, several modelling techniques
which incorporate presence data only have
been developed in recent years (e.g., BIO-
CLIM, Austin et al. 1994; GARP, Peters &
Thackway 1998; ENFA, Hirzel et al. 2002). In
this paper, the distribution modelling map has
been computed by ENFA (Ecological Niche
Factor Analysis) using the software Biomapper
(Hirzel et al. 2002). The distribution modelling
map is then called habitat-suitability map.
ENFA allows us to compare the distribution
of ecological values for a presence data set to
the distribution of ecological values for the
whole study area. Species distribution based on
the ENFA factors is then used to compute a
habitat-suitability map (Hirzel et al. 2002).
Model validation is achieved in Biomapper
through a jack-knife cross-validation process
(Fielding & Bell 1997) with presence points
partitioned in ten subsets of equal sizes.
The study area comprises the world-wide
land area, excluding Antarctica. All analyses
have been performed within a raster-map data
structure based on the latitude/longitude
coordinate system with a 0.5 decimal degree
resolution. The Ilex presence dataset origi-
nated from a tropical American Aquifoliaceae
database (Conservatoire et Jardin botaniques,
Geneva) based on herbarium specimens. The
study included 3506 individuals and each was
described by its geographic coordinates. Only
one location occurring in the same 0.5 x 0.5
degree grid cell was kept, the final sample size
was thus reduced to 826 occurrences. The sec-
ond type of data required for the ENFA is a set
of quantitative raster maps describing the envi-
ronment. A mean monthly climate dataset
(CRU global climate dataset, New et al. 1999)
was used to create annual climatic predictors.
Monthly data consisted of data to 0.5 degree
latitude/longitude resulting from an interpola-
tion from worldwide meteorological stations.
Annual data have been produced through GIS
calculation, resulting in 12 GIS layers.
Pollen fossil distribution
A database of the pollen fossil records for Ilex
from all over the world has been compiled
from published sources cited by Martin (1977),
Muller (1981) or directly from Wijninga and
Kuhry (1993). The data were mapped at world
scale (Scotese 2003) at various geological peri-
ods with for each period the corresponding
position of the continents. The object was to
analyse the distribution of fossil records in an
attempt to determine the origin and phytogeo-
504 BS 55
BS 55 505
Fig. 2. Strict consensus of 22 most parsimonious trees
(820 steps, CI = 0.20, RI = 0.42) obtained from the
matrix of characters using the heuristic search (TBR,
100 random taxon additions) of PAUP. Bootstrap values
(if > 50) are indicated below the branches. Abbrevia-
tions of the geographic distribution are alphabetically:
Afr = Africa, And = Andes, Bra = Brazil, Cam = Central
America, including South Mexico, Can = Canary
Islands, Car = Caribbean Islands, Eas = East Asia, Eur =
Europe, Gui = Guiana, Haw Tah = Hawaii/Tahiti, Mac =
Macaronesia, Nam = North America, Sam = South
America, Sea = South-East Asia.
graphic relationships of modern Ilex distribu-
tion. The macrofossils were not retained
because they are not considered a reliable data
source unless they are identified through
autapomorphies shared with extant species
(Hill 2001).
Results
Morphological analyses
The morphological tree (Fig. 2) is incongruent
with either the plastid or nuclear tree. The
Consistency Index (CI) of each character was
calculated on the plastid and nuclear trees to
determine any correlation between morpho-
logical characters and molecular trees. No cor-
relation was found with any of the molecular
trees (results not shown).
Distribution modelling map
The genus Ilex shows a global marginality value
of 0.939 and a global tolerance value of 0.292,
indicating as expected that its habitat differs
from the world average conditions and that its
ecological niche is relatively restricted. The
first four ENFA factors account for 92% of the
variance. The marginality factor alone explains
72% of the variance. Its coefficients show that
Ilex distribution is essentially linked to indices
of precipitation (0.49 for the year, and 0.41 for
both the driest and wettest months) and to a
lesser extent temperature during the coldest
month (0.33) and number of frost days
(- 0.31). The suitability map is based on all the
ENFA factors. The jack-knife cross-validation
shows that predicted suitability exceeds 0.5 in
69.6% of the validation cells, which proves that
the model is well supported.
506 BS 55
Fig. 3. Habitat-suitability map for Ilex, as computed by Ecological-Niche Factor Analysis (ENFA). Ilex occurrences from
which ENFA was computed are illustrated with black dots. The habitat suitability values are represented as follows: white
areas 0-20%, light-gray areas 20-40%, gray areas 40-60%, dark-gray areas 60-80% and black areas 80-100%. Hatched areas
correspond to the extant distribution of the genus. The model accuracy is given by the strong values of the mean (65,53)
and the standard deviation (28,04) of values predicted by the model for the occurrences.
The map of potential distribution obtained
(Fig. 3) is consistent with the distribution of
the genus at present. However, due to all the
geographical occurrences being from Central
and South America, the model has a lesser pre-
dictive probability for the northern hemi-
sphere (sampling bias). Nevertheless, the
model is sufficiently relevant to allow an inter-
pretation of the differences between potential
and observed distribution compared to the
paleo-environmental variations.
Pollen fossil distribution
Pollen fossil records have been plotted from
the Mid-Cretaceous through to the Miocene.
Figure 4 shows the geographical distribution of
Ilex fossil records at different geological peri-
ods considering continental drift.
Discussion
Past species diversity
Palynological data indicate only the presence
or absence of the genus in a place at a given
time, but give no information on the specific
diversity of Ilex in the past as the species cannot
be distinguished based on pollen morphology
only. In terms of distribution of the occur-
rences in space and time, such records do not
give any information on the migratory path-
ways or the centres of diversity.
As outlined by Cuénoud et al. (2000), pollen
fossil records taken from the literature seem to
indicate that the Ilex lineage was already cos-
mopolitan long before the end of the Creta-
ceous. Cuénoud et al. (2000) and Manen et al.
(2002) arrived at the conclusion that the origin
of Ilex is c 50 mya, on the basis of phylogenetic
study of extant taxa. They do not dispute the
possibility that older ancestors existed, but
those would belong to currently extinct
branches.
The high homogeneity of extant species of
the genus, in spite of at least 50 million years of
evolution and a very broad distribution, sug-
gests that speciation within the genus is very
slow (but see Burnham & Graham 1999).
Differentiation of extant Ilex species
The very complex history of the genus Ilex is re-
flected in our incapacity to produce a relevant
cladogram of morphological characters, which
is also underlined by the incongruence ob-
served between the plastid and nuclear phylo-
genies. The great potential of inter-specific hy-
bridization of Ilex (Galle 1997), associated with
multiple migration pathways defined by Cué-
noud et al. (2000) could explain our incapabili-
ty to achieve a hierarchical arrangement of the
species. It thus appears to be impossible to use
the evolutionary tendencies of the genus to
analyse the cladograms on a hierarchical basis.
Several studies of wood anatomy (Baas 1973),
leaves (Baas 1975), and pollen (Lobreau-Callen
1975; Martin 1977), show that it is impossible to
distinguish the different species on the basis of
these characters. Furthermore, these authors
observed great homogeneity within the extant
species throughout the world.
At a morphological level, the extant species
are often defined by continuous variation of
forms and/or dimensions. Within the study of
South American species, the difficulty over sep-
arating the different species has not been
resolved. Often, the samples can be classified
on a gradient which passes imperceptibly from
one species to the other (e.g., Ilex kunthiana
Triana, I. myricoides Kunth, I. ovalis (Ruiz &
Pav.) Loes., I. rupicola Kunth, I. scopulorum
Kunth, I. uniflora Benth.). A biometric study in
progress on Ilex laurina Kunth, I. yurumanguinis
Cuatrec. and I. maxima W. J. Hahn confirms
the existence of this gradient without the possi-
bility of morphologically separating them with
the exception of the typical specimens of each
taxon. A certain number of samples could be
interpreted as being hybrids between I. laurina
and I. yurumanguinis.
BS 55 507
508 BS 55
Fig. 4 (A-B). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-
tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). A) Miocene. B) Oligocene. The
periods of time corresponding at the position of the continents are: A) 10 mya. B) 30 mya.
BS 55 509
Fig. 4 (C-D). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-
tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). C) Eocene. D) Paleocene. The
periods of time corresponding at the position of the continents are: C) 40 mya. D) 60 mya.
510 BS 55
Fig. 4 (E-F). Ilex fossil distributions at different geological periods. Position of landmasses according to Scotese 2003. Posi-
tion of pollen according to Martin (1977), Muller (1981) and Wijninga and Kuhry (1993). E) Late Cretaceous. F) Mid-Cre-
taceous. The periods of time corresponding at the position of the continents are: E) 70 mya. F) 90 mya.
These facts suggest that the number of
extant species of Ilex could be greatly reduced
after taxonomic study.
Extant distribution
A disjunct distribution pattern is observed
between eastern Asia and eastern North Amer-
ica, as there are no Ilex species along the west-
ern North American coast. This disjunct distri-
bution pattern has been known for many years
and for numerous taxa (Graham 1972; Raven
1972; Raven & Axelrod 1974; Boufford &
Spongberg 1983).
This general phytogeographical pattern can
be directly explained by the broad distribution
of elements of northern hemisphere forests
during the mid-Tertiary and subsequent
colonisations in north-western America and
western Europe in response to climatic cooling
at the end of the Tertiary and during the Qua-
ternary (Wen 1999). The Bering and northern
Atlantic land bridges probably contributed to
the floristic exchanges between southeastern
Asia and North America. Tiffney (1985) pro-
posed five possible principal periods for these
exchanges: Pre-Tertiary, beginning of Eocene,
end of Eocene-Oligocene, Miocene, and the
end of the Tertiary-Quaternary.
In eastern Asia, the majority of genera with a
disjunct distribution between southeastern
Asia and eastern North America are present in
the Sino-Japanese floristic area (Boufford
1998). This area extends from western Yunnan
and Sichuan, through eastern and southern
China, to eastern Korea and Japan (Wen
1999). The Sino-Japanese area is additionally
rich in endemics (Wen 1999).
Ilex seems to follow this pattern of distribu-
tion for the eastern and south-eastern Asian
and North American species. In the former
area great species diversity is found whereas in
the latter only few species occur. It is interest-
ing to note that deciduous species are only pre-
sent in North America and eastern Asia. The
Bering land bridge probably allowed the pas-
sage of deciduous taxa of Ilex for a longer
period of time than for the evergreen ones,
because of the capacity of deciduous species to
survive in a colder climate by losing their
leaves. The deciduous species seem to be the
most recently evolved as an adaptation to the
cool periods that appeared during the late Ter-
tiary. But no information is available that
would allow us to know when deciduous taxa
appeared, or on which continent, or if they
appeared separately on each continent. Plastid
data suggest it happened twice, both in North
American/Asia disjunctions.
Wen (1999) showed that most intercontinen-
tal species pairs are not sister species, which
could mean that species pairs found in both
continents do not necessarily have a direct phy-
logenetic link. Three reasons could be invoked
to explain this morphological similarity: (1)
the pairs of species have been separated for a
very long time and did not evolve much before
or after their separation (Wen 1999), and a
morphological “dormancy” theory (stasis) is
suggested to explain this, (2) the morphologi-
cally similar species are the product of similar
evolution in distant, but equivalent environ-
ments. Qiu et al. (1995) believe that the similar
type of habitat can exert a comparable pres-
sure, which influences in a convergent way the
morphological adaptation, and 3) pairs of
species are not so morphologically similar as
previously suggested.
These observations could explain why the
plastidic, nuclear and morphological phyloge-
nies of the Ilex are not congruent.
The specific relations between North Amer-
ica and south-eastern and eastern Asia should
be studied more deeply to see if sister species
are present on these two continents. Some of
the deciduous Ilex species living on one conti-
nent are considered to be close to species liv-
ing on the other continent by Galle (1997).
This suggests that these species could be sister.
BS 55 511
In the plastid phylogeny, deciduous species are
limited to Asian/N. American clades I and II
(Manen et al. 2002). However, this character
does not seem to prevent interspecific
hybridizations between deciduous and ever-
green species. Thus Galle (1997) observed pos-
sible natural hybridisations in seedling beds
between two North American species: I. decidua
Walter (deciduous) and I. opaca Aiton (ever-
green).
Potential distribution
The current distribution of Ilex seems to be
directly related to precipitation, minimum
temperatures and number of frost days. The
projection of the world potential distribution
calculated on the basis of tropical American
occurrences (Fig. 3) gives a map which largely
resembles the current distribution of Ilex, if
one considers a potential distribution between
20% and 100% of habitat suitability. However,
differences are observed in Europe and South
Africa, which have a potential area of distribu-
tion smaller than actual, and along the west
coast of Canada, southern coast of Chile, New
Zealand and eastern coast of Australia, where
the potential distributions are larger than the
extant ones.
Because of the differences in seasonality
between the northern and the southern hemi-
spheres, only the monthly averages of the
month which expresses an annual limit of a
given climatic variable were considered. Thus
for example it is the monthly average of the
coldest month for each point independently
through all the twelve months which is used to
establish the layer of the minimum tempera-
ture. Our model could have been more precise
considering each month as a variable. But as
our presence data cover primarily the tropics
of Central and South America, a model using
all monthly averages would have increased the
area of potential distribution for the habitat
suitability values between 80% and 100% in the
southern hemisphere, whereas it would have
decreased it in the northern hemisphere. To
correct this artifact due to sampling bias in the
southern hemisphere it would be necessary to
reverse monthly data in the northern hemi-
sphere, i.e. to make it coincide between the
seasons of both hemispheres.
Ilex is a genus represented by plants growing
in relatively wet places and is mostly found in
forests (Martin 1977). Even if Ilex sometimes
grows in drier areas, e.g. on tops of hills in the
centre of primary forests, or in secondar y forest
formations, or in savannas, the genus is always
near water (forest gallery, swamp). Thus Ilex
seems to be able to survive in drier types of veg-
etation if it receives a water complement. As a
consequence even if the potential distribution
is more restricted than the extant one, particu-
lar local climatic conditions approaching opti-
mal ones would allow the genus to survive in ar-
eas indicated as unfavourable at the resolution
of the map. These particular climatic condi-
tions cannot appear on a potential map of dis-
tribution using 0.5° square pixel. These micro-
climatic conditions could explain the occur-
rences of Ilex where the ecological niche proba-
bility is low. However, it seems that the thresh-
old of 20% of habitat suitability is the lower lim-
it in our modelled pattern to find an Ilex plant.
Our modelled pattern corresponds rather
well to the reality of the potential distribution
of the genus. It requires improvements by
introducing more events, particularly in the
northern hemisphere and temperate areas,
and by adding other climatic variables. How-
ever, general differences between the model
and the observed distributions could also be
the result of earth’s climatic history which, will
be discussed further.
Migration
Because the fruit of Ilex is adapted to bird dis-
persal and the embryo can take between 2 to 8
years to germinate (Galle 1997), conditions for
512 BS 55
successful long-distance dispersal are met. Tak-
ing into account the study of Myking (2002) on
the dissemination of Ilex aquifolium L., the
genus Ilex would take 100,000 years to migrate
around the earth under good conditions by
terrestrial pathways. Bird-effected dispersal
highly accelerates this speed, and moreover
makes it possible to place the seeds directly
into favourable biotopes, since the birds tend
to seek similar climatological conditions and
biotopes throughout their migration. Crossing
oceans can be achieved by birds in a few days
(Schlüssel pers. comm.). Alerstam (1990) indi-
cated a 20-hour, non-stop flight to cross the
Gulf of Mexico (1000 km) for the Turdidea
(typical Ilex fruit dispersors) in their migration
way from United States to Yucatán. In addition,
the probability that a seed carried by the
marine currents can cross is weak but exists.
Paleogeography
Broad distribution of pollen of Ilex at the end
of the Cretaceous and throughout the Tertiary
suggests that this genus was widespread at that
time. Projection of pollen fossil occurrences
on paleo-environmental maps drawn from
Beerling and Woodward (2001) (data not
shown) showed that in the late Cretaceous, as
in the Eocene, Ilex was found in zones sup-
posed to have at least 20° C minimum averages
annual temperature and monthly precipitation
average of 100-125 mm. These are coarse data
and thus represent only tendencies in tempera-
ture and rainfall variables. But they correspond
relatively well to the ecological preferences
observed for extant species.
The oldest Ilex pollen, from Australia, was
dated to be from 90 mya. There are five
records of Ilex in the Cretaceous, which are dis-
tributed in Africa, southeastern Australia,
northwestern Borneo, California and former
U.S.S.R. These data do not give any indication
on the place of origin of the genus. Although
data on Cretaceous Ilex fossils should be con-
firmed, nevertheless, one must wonder how
this genus could have been so widespread at
that time, since the continents were already
quite separate.
A first assumption would be that the genus
Ilex is even older, and that its origin goes back
to the time when the continents were still
united (early Cretaceous). Willis and McElwain
(2002) in particular place the origins of the
angiosperms approximately 140 mya. It is
strongly unlikely that the genus Ilex, as recog-
nised today, was already present at that time.
APG (1998) places the Aquifoliaceae in a basal
position of the Asterideae, which suggests a
much more recent appearance of this family
within the angiosperm phylogeny.
The current distribution pattern of the
genus Ilex and the available palynologic data
suggest an Arcto-Tertiary origin of the family.
The current distribution of diversity centres
would thus be directly related to the evolution
of paleo-environmental conditions. The genus
would have disappeared from the continents
which would have undergone cooling events
during Miocene until the glaciations of the
Quaternary. The study of paleo-environmental
models (Beerling & Woodward 2001) lead us
to believe that no climatic variation, besides
that of the Quaternary between 25,000 and
15,000 years ago could have been the cause of
the extinction of some species of Ilex from cer-
tain areas of the world, e.g. Europe, Africa or
New Zealand, where specific diversity is very
low for the first two areas and null for the last
(no extant Ilex in New Zealand). Paleo-environ-
mental considerations are discussed further,
and references are drawn from Adams (1997)
and Adams and Faure (1997).
Eurasia – In the Tertiary, pollen of Ilex was
found throughout Asian continent and the
genus was widespread from Europe to China.
During the Quaternary, conditions all over
northern Eurasia appear to have been dry and
the continent was treeless. It was dominated by
BS 55 513
polar desert or semi-desert steppe-tundra.
These conditions also extended towards the
south in Europe, western and central Asia. In
both tropical and temperate southern Asia
conditions were much drier and colder than
now, with diminished areas of forests and
expanded areas of desert. It thus seems that
these climatic conditions made it possible for
Ilex to survive in certain areas. The climatic
changes did not completely extinguish the
extant species, but instead probably isolated
them in refugia. This isolation may be the
cause of the large number of species in south-
eastern and eastern Asia today. Isolation could
create conditions for allopatric speciation
events without a complete genetic separation
of the species, which would maintain the
potential of inter-specific hybridisation in the
case of Ilex. With later climatic warming the
taxa would again come into contact and
hybrids appeared. South-eastern Asia became
the region which offered the most refugia dur-
ing the successive cooling periods of the Qua-
ternary. It has been considered as the center of
origin for Ilex by Hu (1967), but this has not
been confirmed by the palynological studies
which show Ilex was already widespread (Mar-
tin 1977).
The high specific diversity in this area could
have two causes which do not exclude each
other: 1) the rate of extinction in the genus
was weaker in south-eastern Asia than in other
areas of the world due to greater availability of
refugia during the Quaternary and 2) a greater
number of sister species were derived by
allopatric speciation during periods of expan-
sion and regression of refugia and later by
hybridization of taxa when they came back into
contact.
During the Tertiary, Europe was covered by
an Arcto-Tertiary flora which included Ilex. A
lot of Ilex fossil pollen grains have been found
from this period. During the Quaternary, cli-
matic conditions were extreme, very cold and
very dry, and it is supposed that Ilex was mostly
absent from the continent. Only four species
are found in Europe (including the Canary
Islands, Madeira and Azores) today, Ilex
canariensis Poir., Ilex colchica Pojark., Ilex perado
Aiton,and Ilex aquifolium L., which are all
closely related. A common ancestor could have
been the only survivor of the glaciations. It may
have found refuge in the south of Spain
and/or in the Canary Islands. If conditions
excluded its survival during the Quaternary its
presence could be the result of a recolonisa-
tion. The four species present in Europe,
although they are quite isolated from each
other are nevertheless relatively close to each
other in their morphology. This could mean
that they result from a unique taxon that was
widespread during the Tertiary and which
would have survived in disjunct areas during
the Quaternary.
North America – During the Tertiary, fossil
Ilex pollen was present on the North American
continent. The presence of the Quaternary ice
sheet implies that Ilex was absent from all over
northern North America, nevertheless some
species may have existed in refugia in the
forests of the south-east (Webb & Overpeck,
http://web.ngdc.noaa.gov/paleo/image/-
gsafinal.gif). Availability of refuge areas could
be an important factor in the diversification of
the species and therefore, could explain the
absence of Ilex in western North America
despite a potential distribution along the west-
ern coast of Canada.
Central and South America – Central America
was formed relatively recently (Burnham &
Graham 1999) and no Ilex pollen older than 10
mya has been found. On the other hand, in
South America, three Ilex pollen stations of 40
mya in the north and 60 mya in the south have
been found. We can conclude that the genus
was present in South America before the junc-
tion with North America was formed. A signifi-
cant event on the South American landmass is
514 BS 55
the uplift of the Andes. The presence of Ilex
pollen at the beginning of the uplift of the
Andes allows us to suppose that the genus
shifted up with the uplift of the Andes. Gradu-
ally climatic conditions changed and some
populations were isolated in valleys by high
mountains, allowing for allopatric speciation.
It seems that Quaternary cooling did not
have such an important influence on Central
and South America as it did on Europe and
North America. Central and South America
probably had refugia in the tropical forests,
such as in Panama and the Amazonian basin.
The connection between the Andes and Cen-
tral America probably allowed the Andean
species, driven out by unfavourable climatic
conditions in the Quaternary, to take refuge in
less arid areas of Central America. The Andean
uplift and the extensions and regressions of
favourable habitats during the Quaternary and
the absence of desertification probably sup-
ported specific diversity of Ilex in this region.
Australia and New Zealand – Ilex pollen from
southern and eastern Australia has been found
from the Tertiary and in New Zealand from the
middle Tertiary. During the Quaternary,
species took refuge in the northern Australia
(Martin 1977). At that time the centre of Aus-
tralia became a desert and the south-eastern
forest went extinct. A bridge connected Aus-
tralia to New Guinea. Some rain forests proba-
bly survived in New Guinea and in the far
north of Australia implying potential refugia
for Ilex. In New Zealand forests probably disap-
peared completely leading to the extinction of
the genus in these islands.
Africa – It is surprising to note that very few
Ilex pollen grains have been identified from the
Tertiary of Africa. Only two occurrences are
known, dated 85 mya and 5 mya, respectively.
Nothing indicates that the climate during the
Tertiary or Quaternary in Africa could have led
to the extinction of the genus. Indeed, during
the coldest period of the Quaternary refugia
for tropical forests, and in drier areas for
gallery-forests, existed. In spite of that, the
genus is represented only by one species, I.
mitis (L.) Radl. This single species is found in
the southern part of the continent south of
equator, excluding the desert regions of south-
western Africa. It is also present in Madagascar.
A first hypothesis could be that Ilex was not
widespread in Africa during the Tertiary and
that it was only present in areas that underwent
the strongest climatic variations during the
Quaternary. Another hypothesis would be that
Ilex species were widespread during the Ter-
tiary, but species were not isolated in refugia
during the cooling periods and they were
almost eliminated at that time, and/or later,
during the cooling periods of the Quaternary.
The genus would finally almost disappear from
this continent, Ilex mitis being the only species
to survive.
But if all species of Ilex were eliminated from
Africa, its presence could still be the result of a
subsequent colonisation. The fact that I. mitis is
well established in Madagascar could also sug-
gest a colonization of continental Africa from
this island. The Malagasy flora seems to pass
more easily from the island to the African con-
tinent than the opposite. In addition, the ori-
gin of a great number of Malagasy species
could be Asia, due to favourable marine cur-
rents which cross the Indian Ocean and which
would support long distance dispersal (Gautier
pers. comm.). This could explain why I. mitis is
close to a certain number of Asian species in
the nuclear and plastid clades (Manen et al.
2002). Additional studies are needed.
Conclusions
The genus Ilex was probably widespread from
the beginning of the Tertiary, and perhaps
before. The first Ilex pollen fossils are dated
older than 85 mya, and were found in Africa,
Australia and Asia. Consequently it is impossi-
BS 55 515
ble to have an idea of the origin of the genus
on the basis of palynological studies. In addi-
tion, a calculation based on the molecular
clock for the extant Ilex species gives an origin
of approximately 50 mya. This is interpreted as
being the age of the oldest ancestor of the cur-
rent species. Any trace of even older ancestors
is lost with the extinction of the branches
which corresponded to them.
The study of the extant species shows a great
homogeneity of floral morphology within the
genus in spite of, according to the molecular
clock, approximately 50 million years of evolu-
tion. This fact suggests a “morphological sta-
sis,” that is to say a great stability of characters
over a very long time period. In addition, it
seems that different species hybridize leading
up to morphological and molecular homo-
geneisation. This apparent great stability of
characters and the possibility of hybridisation
makes the elucidation of relations between
species even more difficult.
Attempts to reconstruct phylogenies of
extant species based on sequencing of plastid
and nuclear DNA, confirm the potential to
hybridize. A phylogeny based on morphologi-
cal characters was not resolved and brought no
new information to the problem. Comparison
between morphological characters and plastid
phylogeny, which seemed to give the most sig-
nificant results compared to the nuclear one,
showed that there was no correlation between
them. All the above mentioned factors high-
light the enormous difficulty encountered
when attempting to connect the evolutionary
history of the genus with the extant distribu-
tion, and in determining centres of origin for
the genus. Information currently available can-
not give any indication of the number of
species present in the past, and it gives only a
few indications of possible migratory pathways
of these species according to extant distribu-
tions.
A statistical analysis based on specimen
records in our database (more than 3500 indi-
viduals from Central and South America)
made it possible to propose a potential distrib-
ution of the genus Ilex. The potential distribu-
tion corresponds, in the broad outline, to the
extant distribution except for some areas in
western North America and in Africa. The
assumption made is that the genus was wide-
spread at the end of the Tertiary and that it has
been restricted to the current distribution due
to colder and drier climatic conditions during
the Quaternary. The very high number of
species in south-eastern Asia and South Amer-
ica could be directly related to these two areas
acting as refugia during the Quaternary, and to
the slow uplift of the Andes during the Tertiary
in South America.
The situation seen in Africa is not clear.
Either Ilex was never widespread on this conti-
nent during the Tertiary, or it was widespread
but climatic conditions of the Quaternary were
more drastic than currently knowledge sup-
poses implying widespread extinction in Africa
(Raven & Axelrod 1974).
To improve our knowledge of Ilex distribu-
tion patterns, it will be necessary to work on
several levels:
Complete the pollen data, particularly for
South America and Africa. In addition, it
would be interesting to have information
about the presence of Ilex in the Antarctic dur-
ing the Tertiary (Partridge pers. comm.).
Improve our knowledge of the pattern of
potential distribution by integrating data from
temperate zones of the northern hemisphere,
and increasing the number of climatic vari-
ables. This will better define the ecological
niche and allow us to compare it to paleoenvi-
ronmental patterns.
Improve our knowledge of species variability.
This will allow us to have a better understand-
ing of the different taxa and clarify better their
current distribution patterns.
516 BS 55
Acknowledgements
We thank all the herbaria mentioned in the
text for kindly lending us Ilex material; Cyrille
Chatelain for his invaluable council concern-
ing GIS; Michelle Price for checking the Eng-
lish text, André Schlüssel for suggestions dur-
ing the drafting of the manuscript.
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BS 55 519
Appendix 1: The 47 Ilex species selected for the morphological phylogeny. Descriptions were based on cited literature and
speciminens seen which are indicated with the collector, the collector’s number, the acronym of the herbarium and their
sexual status (f: female, m: male, st: sterile).
Taxa Literature and Specimens seen
I. amelanchier M. A. Curtis Loesener 1901, Galle 1997, Drummond s.n. 1832 BM f, Leonard 1728 BM f, Curtis s.n. 1852
G f
I. anomala Hook. & Arn. Loesener 1901, Galle 1997, Faurie 282 G mf, Degener 20061 G f, Degener 3316 G m, Degener
3324 G m,
I. argentina Lillo Galle 1997, Beck 9660 G m, Venturi 4623 S m, Giberti 508 G f, Venturi 9990 S f
I. brasiliensis (Sprengel) Loes. Giberti 1994, Regnell II 56 S m, Mosén 4243 S f, Mosén 1822 S f
I. brevicuspis Reissek Giberti 1994, Balansa 1793 S f, Hatschbach 30782 MU m
I. canariensis Poir. Loesener 1901, Galle 1997, Mandon s.n. 1865-1866 G m, Mason 349 G f, Asplund 1112 G m
I. cassine L. Galle 1997, Standley 190 BM f, Tracy 6829 BM mf, Drummond s.n. BM st, Curtiss 1747 BM m
I. crenata Thunb. Loesener 1901, Galle 1997, Anonymous 155 G m, Kasapligil 3660 G f, Faurie 3114 G m
I. decidua Walter Loesener 1901, Galle 1997, Ventenat s.n. G m, Godfrey 54470a G m, Eisenbeiss & Dudley s.n.
1979 G f, Bosc s.n. G f, Godfrey 54549 G f
I. dumosa Reissek Giberti 1994, Schinini 31582 G m, Hatschbach 22945 S m, Schinini 31420 G f
I. glabra (L.) A. Gray Galle 1997, Bartram 445 BM mf, Bray 8423 BM m, Rugel 3365 BM f
I. goshiensis Hayata Galle 1997, Furuse 2498 G m, 2768 K f, 2959 K m, 3550 K f
I. guianensis (Aubl.) Kuntze D’Arcy &al. 15500 G m, 15506 G m, Churchill 4284 G m, Gentry & al. 47534 COL m, 47555
COL f, Werff, van der &al. 6153 G f, 6916 G m
I. hippocrateoides Kunth Humboldt & Bonpland s.n. P m, Núñez & al. 9034 G st, 9904 G f, Hamilton & Holligan 661
K st, Smith 2723 G f
I. integerrima (Vell.) Reissek Loesener 1901, Freyreis s.n. S f
I. latifolia Thunb. Loesener 1901, Galle 1997, Maximowicz s.n. G mf
I. laurina Kunth Bernardi 1045 NY m, Sneidern 4356 F m, Lehmann B.T.668 G, NY m, B.T.959 NY f, Williams
6995 COL, F f, Cuatrecasas 18281 F, G, US f, Humboldt & Bonpland s.n. W m
I. leucoclada (Maxim.) Galle 1997, Wilson 7099 BM mf, Wilson 7630 BM f
Makino
I. liebmannii Standl. Standley 1931, Galle 1997, Liebmann 14927 G f (fragments).
I. longipes Trel. (= I. collina) Loesener 1901, Galle 1997, Nogle s.n. 1956 BM f, Dudley s.n. 1976 BM m, K f
I. macrocarpa Oliver Loesener 1901, Galle 1997, Linsley Gressitt 1736 G f
I. macropoda Miq. Loesener 1901, Galle 1997, Tschonoski s.n. 1864 G mf, Watari s.n. 1951 G f, Anonymous s.n.
1888 G m, Nagamasu 5457 G m
I. maximowicziana Loes. Loesener 1901, Galle 1997, Furuse 3400 G m, Furuse 1060 K f, Furuse 2883 K f,.
I. micrococca f. pilosa S. Y. Hu Galle 1997 (I. micrococca), Henry 11974a K f, Fang 5656 K f, Forrest 8651 K f, 15749 K m
I. microdonta Reissek Hatschbach 24206 S f, 22837 COL m
I. mitis (L.) Radlk. Galle 1997, Pegler 1366 BM m, Zeyher 1129 BM m, Bolus 5202 BM mf, Drege s.n. BM mf
I. mucronata (L.) M. Powell, Loesener 1901, Chapman s.n. 1844 G m, Pringle s.n. 1877 G f, Cinq-Mars 67-54 G m
V. Savolainen & S. Andrews
520 BS 55
Taxa Literature and Specimens seen
I. mutchagara Makino Furuse 4812 K m
I. oppositifolia Merrill Galle 1997, Clemens 31108 BM f, 31375 BM st, 32249 BM f, 40539 BM m
I. pedunculosa Miq. Galle 1997, To Hara 2441 K m, Maximowicz s.n. K mf, Murata 15833 K f
I. perado Aiton Galle 1997, Loesener 1901, Reverchon 76 G f, Mason 343 G st
I. pseudobuxus Reissek Loesener 1901, Mosén 2898 S m, 3651 S f, Britez 1397 MBM f, Tessmann s.n. 1953 MBM m
I. pubescens Hook. & Arn. Loesener 1901, Galle 1997, Shiu Ying Hu 8996 G f, Tso 20100 G m, Lingnan 12016 G f
I. purpurea Hassk. Loesener 1901, Galle 1997, Chiao 1683 G f, Nagamasu 5516 G f, 5524 G m
I. repanda Griseb. Wright 1142 BR f, Wright 1142 K mf, Curtiss 88 K mf, Jack 4835 K f
I. revoluta Stapf Galle 1997, Clemens s.n. BM m, 32315 BM m, Gibbs 9127 BM f
I. rotunda Thunb. Galle 1997, Wright 184 K mf, Furuse 2695 K m, Furuse 2939 K f
I. rugosa F. Schmidt Loesener 1901, Galle 1997, Yatabe s.n. 1882 G f, Tschonoski s.n. 1864 G mf
I. serrata Thunb. Loesener 1901, Galle 1997, Maximowicz s.n. 1862 [Fudziyama] G f, Maximowicz s.n. 1862
[Yokohama] G f, Franchet 178 G m
I. shennongjiaensis Dudley & Sun 1983, Galle 1997
T.R.Dudley & S.C. Sun
I. sugerokii Maxim. Galle 1997, Wilson 7100 K mf, Fukuoka 1052 K m, Maximowicz s.n. K f, Wilson 7183 K f
I. teratopis Loes. Pearce s.n. K mf
I. theezans Reissek Giberti 1994, Dusén 15543 S m, Oliveira 682 MU f, Dusén s.n.1909 S f, Francisco & al.
s.n.1999 G m
I. triflora Blume Galle 1997, Kerr 13277 BM f, 15523 BM f, 17771 BM m, Tsang 29153 G m, Taam 675 G m
I. verticillata (L.) A. Gray Galle 1997, Anonyme s.n. [1824] BM m, Euphrosin s.n. [1926] BM m, Judd s.n. [1932] BM
f, Bauers 4 K f
I. vomitoria Aiton Galle 1997, Rugel 92 BM mf, Hood 1996 BM f, Miller 9460 BM f
I. yunnanensis Franch. Hu 1949, Galle 1997, Delavay 2673 K m, Forrest 10247 K m, Fliegner 1193 K f
