Anagenetic Evolution in Island Plants

ORIGINALARTICLE

Anagenetic evolution in island plants

Tod F. Stuessy1*, Gerhard Jakubowsky1, Roberto Salguero Gomez2, Martin

Pfosser3, Philipp M. Schluter3, Tomas Fer4, Byung-Yun Sun5 and Hidetoshi

Kato6

INTRODUCTION

The origin of new species on oceanic islands has been discussed

on many occasions (Carlquist, 1974; Grant, 1996). The most

commonly described process is speciation associated with

adaptive radiation (Stuessy & Ono, 1998; Schluter, 2000), in

which from a single introduction several lines of speciation

occur, each driven by selection within markedly different

ecological zones. Morphological divergence among species in

this process is often dramatic, but overall genetic differentiation

1Department of Systematic and Evolutionary

Botany, Institute of Botany, University of

Vienna, Vienna, Austria, 2Departamento de

Ecologa Vegetal (Botanica), Universidad de

Sevilla, Sevilla 41012, Spain, 3Biologiezentrum,

Landesmuseum, Johann-Wilhelm-Klein-

Strasse 73, Linz 4010, Austria, 4Department of

Botany, Faculty of Science, Charles University,

Prague 11636, Czech Republic, 5Faculty of

Biological Sciences, College of Natural Sciences,

Chonbuk National University, Chonju, South

Korea and 6Makino Herbarium, Tokyo

Metropolitan University, Hachioji, Tokyo,

Japan

*Correspondence: Tod F. Stuessy, Department

of Systematic and Evolutionary Botany, Institute

of Botany, University of Vienna, Rennweg 14,

A-1030, Vienna, Austria.

E-mail: [email protected]

ABSTRACT

Aim Plants in islands have often evolved through adaptive radiation, providing

the classical model of evolution of closely related species each with strikingly

different morphological and ecological features and with low levels of genetic

divergence. We emphasize the importance of an alternative (anagenetic) model of

evolution, whereby a single island endemic evolves from a progenitor and slowly

builds up genetic variation through time.

Location Continental and oceanic islands.

Methods We surveyed 2640 endemic angiosperm species in 13 island systems of

the world, both oceanic and continental, for anagenetic and cladogenetic patterns

of speciation. Genetic data were evaluated from a progenitor and derivative

species pair in Ullung Island, Korea, and Japan.

Results We show that the anagenetic model of evolution is much more

important in oceanic islands than previously believed, accounting for levels of

endemic specific diversity from 7% in the Hawaiian Islands to 88% in Ullung

Island, Korea, with a mean for all islands of 25%. Examination of an

anagenetically derived endemic species in Ullung Island reveals genetic

(amplified fragment length polymorphism) variation equal or nearly equal to

that of its continental progenitor.

Main conclusions We hypothesize that, during anagenetic speciation, initial

founder populations proliferate, and then accumulate genetic variation slowly

through time by mutation and recombination in a relatively uniform

environment, with drift and/or selection yielding genetic and morphological

divergence sufficient for the recognition of new species. Low-elevation islands

with low habitat heterogeneity are highly correlated with high levels of anagenetic

evolution, allowing prediction of levels of the two models of evolution from these

data alone. Both anagenetic and adaptive radiation models of speciation are

needed to explain the observed levels of specific and genetic diversity in oceanic

islands.

Keywords

Amplified fragment length polymorphism, anagenesis, cladogenesis, endemic

plants, genetic differentiation, habitat heterogeneity, island biogeography, island

evolution, speciation.

Journal of Biogeography (J. Biogeogr.) (2006) 33, 12591265

2006 The Authors www.blackwellpublishing.com/jbi 1259Journal compilation 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01504.x

may be low (DeJoode & Wendel, 1992; Frankham, 1997;

Baldwin et al., 1998; Crawford & Stuessy, 1998; Emerson,

2002). Well-known examples include the lobelioids and

silverswords in Hawaii (Givnish et al., 1995; Carlquist et al.,

2003).

A contrasting mode of evolution is one in which a founder

population arrives on an island and simply diverges through

time without further specific differentiation. This anagenetic

speciation (also known as simple geographic or phyletic

speciation) has been suggested as an important mode of

evolution in the endemic vascular plants of the Juan Fernandez

Islands (Stuessy et al., 1990), but the pattern has not been

studied in other oceanic archipelagos and is less well under-

stood regarding its genetic consequences than is the classical

model of adaptive radiation. The term anagenetic speciation

has been selected for convenience in communication. It is

realized that the source populations could also be undergoing

change, especially if the environment were to be changing

rapidly, for example as a result of Pleistocene events. If

speciation were to occur in the continental region, therefore,

one might label this simply cladogenesis, involving the

production of two new species, one on the islands and one

on the continent. We do not object to this point of view, but it

is likely that in most cases the ecology of the newly formed

islands will be changing faster and more dramatically than that

of the continental source area, and, therefore, speciation may

be occurring in the islands more often or faster than in the

source region. We recognize these definitional problems, but

they should not obscure the main point of this paper, which is

to focus on what is occurring during speciation on the islands

after colonization. We regard the term anagenetic speciation as

useful to contrast with speciation during adaptive radiation,

which clearly involves the splitting of lineages (or cladistic

divergence) in a more dramatic fashion.

This report surveys the angiosperm floras of 13 island

systems, of both oceanic volcanic (Canary, Cape Verde,

Galapagos, Hawaii, Juan Fernandez, Madeira, Ogasawara, St

Helena, Tristan da Cunha, Ullung) and continental (Chatham,

Falklands, Taiwan) origins, revealing that anagenetic speciation

conservatively explains 25% of the total endemic species

diversity. We seek correlations with physical and environmen-

tal parameters that might explain observed levels of the two

patterns of speciation within each island or archipelago. We

also offer a hypothesis, based on available data, for genetic

consequences of the anagenetic speciation model.

METHODS

A data base of 2640 endemic species for the island survey was

prepared from published floras for 13 island systems plus

additional literature: Canary Islands, Wildpret de la Torre &

Del Arco Aguilar (1987), Coello et al. (1992), Hansen &

Sunding (1993); Cape Verde Islands, Bernard-Griffiths et al.

(1975), Boekschoten & Manuputty (1993), Brochmann et al.

(1997); Chatham Islands, Wills-Johnson et al. (1996); Falkland

Islands, Moore (1968), Lawrence et al. (1999); Galapagos

Islands, Wiggins & Porter (1971), Hamann (1981), Perry

(1984); Hawaiian Islands, Wagner & Funk (1995), Wagner

et al. (1999); Juan Fernandez Islands, Skottsberg (1953),

Stuessy et al. (1984), Marticorena et al. (1998), Greimler et al.

(2002); Madeira, Press & Short (1994), Hughes & Malmqvist

(2005); Ogasawara Islands, Ono & Okutomi (1985), Takayama

et al. (2005); St. Helena, Cronk (2000); Taiwan, Huang (1994),

Huang et al. (2004); Tristan da Cunha Islands, Wace &

Holdgate (1958), Wace (1961), Miller (1964), Gass (1967),

Groves (1981), McDougall & Ollier (1982), Roux et al. (1992);

Ullung Island, Kim (1988), Sun & Stuessy (1998).

Data on natural vegetation types, ages of islands, and other

environmental parameters were taken from the literature cited

above. Comparing vegetation heterogeneity among archipela-

gos is difficult because different systems of classification of

vegetation are in use. We extracted from the literature the

number of vegetation types of comparable hierarchical level

from each island/archipelago. To reduce problems of compar-

ability we then grouped the number of vegetation types into

classes: class 1 (14 vegetation types); 2 (58); 3 (912); 4 (13

16); 5 (1720); and 6 (>20).

The most effective way of knowing whether a species has

evolved anagenetically or cladogenetically is by in-depth

studies of each group, including comparisons with continental

progenitors. Such a detailed level of understanding is not

available comprehensively for any island system. For the

purposes of this study, therefore, we have taken a simple

(conservative) approach to estimating levels of anagenetic

speciation. Single endemic species on an island or archipelago

are assumed to have evolved by anagenetic speciation. This

does not account for possible loss of species as a result of

extinction. This is an important point, as it is likely that Pacific

oceanic (and other) islands have undergone considerable

reduction in both surface area and ecological habitat breadth

during their ontogeny, and specific and genetic diversities have

surely been lost (Stuessy et al., 2005). Hence, some single

endemic species may be merely the surviving member of a

once larger endemic group. Unfortunately, without fossil

evidence, which is rarely available from plants on islands, it is

simply impossible to determine levels of extinction in partic-

ular groups. Two or more endemic species in a genus within an

island or archipelago are regarded as reflecting cladogenesis, if

the assumption is made that they both have descended from

the same continental introduction. This ignores possible inter-

island anagenesis, and therefore our approach doubtless

underestimates this mode. Endemic monotypic genera have

also been treated as reflecting anagenesis, even though it may

be the case that some of these related genera may represent

radiating lines from one original ancestor to the islands.

In addition to the above analysis, we present analyses of

genetic variation in populations of Dystaenia (Apiaceae) from

Ullung Island and Japan based on amplified fragment length

polymorphism (AFLP; Vos et al., 1995) data (Pfosser et al.,

2005). A few technical comments are therefore in order. It is

now well accepted that AFLPs can provide a sensitive measure

of overall genetic variation within and among plant

T. F. Stuessy et al.

1260 Journal of Biogeography 33, 12591265 2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

populations (e.g. Tremetsberger et al., 2003; Muellner et al.,

2005). Six populations of Dystaenia takesimana (Nakai) Kitag.

(Ullung Island) and six of Dystaenia ibukiensis (Yabe) Kitagawa

(Japan) were sampled, involving a total of 126 individuals.

These were chosen to reflect the geographic spread of

populations within each species. Total genomic DNA was

extracted from silica-dried leaves following the CTAB protocol

(Doyle & Doyle, 1987), with slight modifications, followed by

standard AFLP protocols (Vos et al., 1995; Tremetsberger

et al., 2004). An initial screening of selective primer combi-

nations yielded three that gave clear and reproducible bands:

EcoRI-ACT/MseI-CAC, EcoRI-ACC/MseI-CTG, and EcoR-

AGG/MseI-CAT. The fluorescence-labelled selective amplifi-

cation products were separated on a 5% polyacrylamide gel

with an internal size standard on an automated ABI 377

sequencer. The data were imported into Genographer (Ver-

sion 1.6.0, http://hordeum.oscs.montana.edu/genographer) for

scoring of the fragments; the results were exported as a

presence/absence matrix for further analysis. The Shannon

index was calculated as HSh )P

(pj ln pj), where pj is the

relative frequency of the jth fragment. Tests for significance of

correlations were calculated with SPSS 8.0 (SPSS, Inc.,

Chicago, IL, USA). Analyses of molecular variance (amovas)

and the coefficient of genetic differentiation (FST) were

calculated with Arlequin 2.0 (Schneider et al., 2000). R

package 4.0 d6 (Casgrain & Legendre, 2001) was used to

perform Mantel tests for each species (10,000 permutations),

comparing the genetic matrix of inter-individual Jaccard

distances with a matrix of geographic distances between

individuals in kilometres.

RESULTS AND DISCUSSION

Table 1 shows levels of anagenetic vs. cladogenetic speciation

in 2640 endemic species of 10 oceanic islands and archipelagos

and three continental islands taken from published floras. The

highest level of anagenetic speciation is for Ullung Island,

Korea, at 88%. At the other extreme are the Hawaiian Islands,

at 7%. The average value for oceanic archipelagos is 22%, and

for continental islands it is 31%. Overall, anagenetic speciation

accounts for approximately one-quarter of all endemic plant

species on these islands.

It is important to emphasize that these values may

underestimate the level of anagenetic speciation in some

archipelagos. For example, the most detailed assessment of

cladogenetic and anagenetic speciation, based on more than

25 years of evolutionary studies on many island taxa, is for the

endemic flora of the Juan Fernandez archipelago (Stuessy et al.,

1990). In this study, anagenesis was estimated as 71%, which is

much higher than the figure given here (36%, Table 1), and

presumably closer to the actual percentage. Another island

where it is possible to give an estimate of anagenesis based on

evolutionary studies is Ullung Island, where the difference is

less. The figure given here is 88% (Table 1), whereas our

previous estimate based on evolutionary studies was 100% (Sun

& Stuessy, 1998; Pfosser et al., 2002). For other archipelagos

with larger endemic floras, however, no detailed summaries are

currently possible. The other archipelago that has received

much recent, especially molecular, attention is the Canary

Islands. Even there, however, only a portion of the endemic taxa

has been examined with modern techniques (Santos, 1998), and

the genetic data are therefore insufficient for a complete

summary of modes of speciation.

The different levels of anagenetic speciation in different

island systems allow a search for correlations with physical

environmental factors (Table 1). No significant correlations

exist with the number of islands in archipelagos, their size, age,

or distance from major source areas, these being traditional

factors used to explain total species diversity (i.e. endemic and

native taxa) on oceanic islands (MacArthur & Wilson, 1967).

Likewise, no significant correlation exists with latitude (not

included in Table 1). Only two factors, elevation and habitat

Table 1 Features of island systems, numbers of endemic species, and levels of anagenetic vs. cladogenetic speciation

Island system

Number of

islands

Size

(km2)

Distance from

mainland (km)

Age

(Myr)

Elevation

(m)

Vegetation

heterogeneity

No. endemic

species

Anagenetic

speciation (%)

Cladogenetic

speciation (%)

Oceanic

Hawaii (H) 8 16,885 3660 5 4250 6 828 7 93

Canary (C) 7 7601 100 21 3710 6 429 16 84

Tristan da Cuhna (T) 4 208 2580 18 2060 3 27 33 67

Juan Fernandez (J) 3 100 600 4 1319 5 97 36 64

Cape Verde (CV) 12 4033 570 10 2829 2 68 37 63

Galapagos (G) 16 7847 930 5 1707 4 133 43 57

Madeira (M) 3 792 630 14 1862 3 96 48 52

Ogasawara (O) 12 99 800 Tertiary 916 3 118 53 47

St. Helena (S) 1 123 1850 15 826 2 36 53 47

Ullung (U) 1 73 130 2 984 2 33 88 12

Continental

Taiwan (TW) 1 35,800 130 5 3950 3 724 29 71

Chatham (CH) 1 963 668 80 294 1 37 62 38

Falkland (F) 2 8500 410 Tertiary 705 2 14 71 29


Journal of Biogeography 33, 12591265 1261 2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

(vegetation) heterogeneity, correlate significantly with this

pattern (Fig. 1a, Pearson two-sided, r 0.84, P < 0.01;Fig. 1b, Pearson two-sided, r 0.77, P < 0.01). Higher islandsgenerally have greater habitat diversity, and this stimulates

cladogenesis and adaptive radiation (e.g. in Hawaii). Lower

islands with more uniform environments yield higher levels of

anagenetic speciation (e.g. in Ullung Island). Hobohm (2000)

has shown a positive correlation of species diversity in the

Macaronesian Islands with elevation and number of vegetation

zones.

The genetic consequences of anagenetic speciation are also

of interest. In the model of adaptive radiation, the original

immigrant gene pool becomes divided as a result of ecological

isolation, and the resultant genetic variation within and among

populations is low (Johnson et al., 2000). Even if a founder-

flush model is advocated (Rundle et al., 1998), the resultant

genetic variation within endemic lineages stays reduced.

Genetic AFLP comparisons of a progenitor-derivative species

pair between Japan and Ullung Island, which shows the highest

level of anagenesis (88%; Table 1), suggest another pattern.

A comparison (Fig. 2) between six populations of D. takesi-

mana (Apiaceae; endemic to Ullung Island) and six of

D. ibukiensis (scattered throughout Japan) fails to show a

reduction in genetic variation (Pfosser et al., 2005) within the

island endemic (number and per cent of polymorphic

fragments, 117.33, 96.17% vs. 103.67, 86.73%, and Shannon

index 33.13 vs. 29.13, respectively). Furthermore, the island

populations all behave as one large island population with no

geographic partitioning of genetic variation (FST 0.014;Mantel test with genetic and geographic distances,

RM 0.042, P 0.15). Based on the AFLP data, each of thetwo populational systems is clearly monophyletic, excluding

multiple introductions for the island endemic. This generic

system was selected because the two taxa are morphologically

distinct (Sun et al., 1997), they have the same breeding systems

(outcrossing, Pfosser et al., 2005), they are the only two species

in the genus, hence eliminating complicating factors such as

hybridization among congeners, and a deletion in the trnL-F

intron and spacer regions in the island taxon strongly suggests

that it was derived from the Japanese species, rather than vice

versa (Pfosser et al., 2005).

Examples of single progenitor-derivative species pairs that

do not fit this genetic pattern, based on allozyme data, include

(1) Rhaphithamnus (Verbenaceae), whereby the Chilean con-

tinental R. spinosus has much more allozymic variation than

the endemic R. venustus of Masatierra Island in the Juan

Fernandez archipelago (Crawford et al., 1993); and (2)

Gossypium (Malvaceae), whereby the Galapagos endemic

G. klotzschianum has less allozymic variation than the

progenitor G. davidsonii from Baja California (Wendel &

Percival, 1990). In these cases, however, it may be that the

reduction of population number and size over several million

years (Cox, 1983; Stuessy et al., 1984) as a result of natural and

human impacts has led to the pattern of reduced genetic

variation now seen (Stuessy et al., 2005). There is also a recent

report (Woo et al., 2002) of reduced allozymic variation in the

Ullung Island endemic Hepatica maxima in comparison with

its Korean peninsula congener H. asiatica. We have examined

(a)

(b)

Elevation (m)0 1000 2000 3000 4000 5000

Anag

enes

is (%

)

0

20

40

60

80

100

Habitat heterogeneity0 1 2 3 4 5 6

Anag

enes

is (%

)

0

20

40

60

80

100

H

C

TJ CV

GM

O S

U

TW

CH

F

H

J

M

CVG

TW

C

T

O

U

CH

F

S

Figure 1 Correlation of anagenetic speciation (%) in endemic

angiosperms of island systems with (a) highest elevation and (b)

habitat (vegetation) heterogeneity. For acronyms see Table 1.

0

10

20

30

40

Shan

non

inde

x

Dystaenia ibukiensisDystaenia takesimana

population size

Population

Sample size

Estimated c. 100 c. 100 500 >1000

this species pair with DNA sequences and AFLP data, however

(Pfosser et al., in press, unpubl. data), and see a similarly high

level of genetic variation in the island endemic to that shown

in Dystaenia. More work on H. maxima and its progenitor will

be needed to resolve this discrepancy.

The equal or higher level of genetic variation seen in

species derived through anagenetic speciation suggests a

mechanism for their origin. After an initial founder event,

the established immigrant population will have greatly

reduced genetic variation. In a favourable uniform environ-

ment, populations will proliferate. Over generations, genetic

variation will accumulate through mutation and recombi-

nation (Lande, 1992) in the isolated island populations as a

result of changes in allelic frequencies through drift and/or

selection (if the island habitat is significantly different from

that of the continent). Lack of eco-geographic partitioning

of genetic variation within the island keeps genetic levels

high. The result is eventually a new species, divergent in

genetic and morphological composition from its progenitor,

but harbouring equal or nearly equal levels of genetic

variation.

ACKNOWLEDGEMENTS

This work was supported by grant P14825-B03 from the

Austrian National Science Foundation (FWF) to T.F.S. and by

the Korean Science and Engineering Fund (KOSEF) to B.-Y.S.

REFERENCES

Baldwin, B., Crawford, D.J., Francisco-Ortega, J., Kim, S.-C.,

Sang, T. & Stuessy, T.F. (1998) Molecular phylogenetic

insights on the origin and evolution of oceanic island plants.

Molecular systematics of plants II. DNA sequencing (ed. by

P.S. Soltis, D.E. Soltis and J.J. Doyle), pp. 410441. Kluwer,

New York.

Bernard-Griffiths, J., Cantagrel, J.M., Matos, C., Mendes, F.,

Serralheiro, A. & Rocha de Macedo, J. (1975) Donnees

radiometriques potassium-argon sur quelques formations

magmatiques des iles de larchipel du Cap Vert. Comptes

Rendus Academie des Sciences Paris (Ser. D), 280, 24292432.

Boekschoten, G.J. & Manuputty, J.A. (1993) The age of the

Cape Verde Islands. Courier Forschungsinstitut Senckenberg,

159, 35.

Brochmann, C., Rustan, .H., Lobin, W. & Kilian, N. (1997)

The endemic vascular plants of the Cape Verde Islands, W

Africa. Sommerfeltia, 24, 1356.

Carlquist, S. (1974) Island biology. Columbia University Press,

New York.

Carlquist, S., Baldwin, B.G. & Carr, G.D. (eds) (2003)

Tarweeds and silverswords: evolution of the Madiinae

(Asteraceae). Missouri Botanical Garden Press, St Louis.

Casgrain, P. & Legendre, P. (2001) The R package for multi-

variate and spatial analyses, version 4.0 d6 users manual.

Departement de Sciences Biologique, University of Mont-

real, Montreal.

Coello, J., Cantagrel, J.-M., Hernan, F., Fuster, J.-M., Ibarrola,

E., Ancochea, E., Casquet, C., Jamond, C., de Teran, J.-R.D.

& Cendrero, A. (1992) Evolution of the eastern volcanic

ridge of the Canary Islands based on new K-Ar data. Journal

of Volcanology & Geothermal Research, 53, 251274.

Cox, A. (1983) Ages of the Galapagos islands. Patterns of

evolution in Galapagos organisms (ed. by R.I. Bowman, R.I.

Berson and A.E. Leviton), pp. 1123. American Association

for the Advancement of Science, San Francisco.

Crawford, D.J. & Stuessy, T.F. (1998) Plant speciation in

oceanic islands. Evolution and diversification of land plants

(ed. by K. Iwatsuki and P.H. Raven), pp. 249267. Springer-

Verlag, Tokyo.

Crawford, D.J., Stuessy, T.F., Rodriguez, R. & Rondinelli, M.

(1993) Genetic diversity in Rhaphithamnus venustus (Ver-

benaceae), a species endemic to the Juan Fernandez Islands.

Bulletin of the Torrey Botanical Club, 120, 2328.

Cronk, Q.C.B. (2000) The endemic flora of St. Helena. Anthony

Nelson, Oswestry, UK.

DeJoode, D.R. & Wendel, J.F. (1992) Genetic diversity and

origin of the Hawaiian islands cotton, Gossypium tomento-

sum. American Journal of Botany, 79, 13111319.

Doyle, J.J. & Doyle, J.L. (1987) A rapid DNA isolation pro-

cedure for small amounts of fresh leaf tissue. Phytochemical

Bulletin, 19, 1115.

Emerson, B.C. (2002) Evolution on oceanic islands: molecular

phylogenetic approaches to understanding pattern and

process. Molecular Ecology, 11, 951966.

Frankham, R. (1997) Do island populations have less genetic

variation than mainland populations? Heredity, 78, 311327.

Gass, I.G. (1967) Geochronology of the Tristan da Cunha

group of islands. Geological Magazine, 104, 160170.

Givnish, T.J., Sytsma, K.J., Smith, J.F. & Hahn, W.J. (1995)

Molecular evolution, adaptive radiation, and geographic

speciation in Cyanea (Campanulaceae, Lobelioideae).

Hawaiian biogeography: evolution on a hot spot archipelago

(ed. by W.L. Wagner and V. Funk), pp. 288337. Smithso-

nian Institution Press, Washington, DC.

Grant, P.R. (ed.) (1996) Evolution on islands. Oxford Univer-

sity Press, Oxford.

Greimler, J., Lopez, P.S., Stuessy, T.F. & Dirnbock, T. (2002)

The vegetation of Robinson Crusoe Island (Isla Masatierra),

Juan Fernandez Archipelago, Chile. Pacific Science, 56, 263

284.

Groves, E.W. (1981) Vascular plant collections from the

Tristan da Cunha group of islands. Bulletin of the British

Museum (Natural History), Botany, 8, 333420.

Hamann, O. (1981) Plant communities of the Galapagos

Islands. Dansk Botanisk Arkiv, 34, 1163.

Hansen, A. & Sunding, P. (1993) Flora of Macaronesia.

Checklist of vascular plants, ed 4. Sommerfeltia, 17, 1295.

Hobohm, C. (2000) Plant species diversity and endemism on

islands and archipelagos, with special reference to the

Macaronesian Islands. Flora, 195, 924.

Huang, T.-C. (ed.) (1994) Flora of Taiwan, Vol. 1, 2nd edn.

Editorial Committee Flora of Taiwan, Taipei.



Huang, S.-F., Hwang, S.-Y., Wang, J.-C. & Lin, T.-P. (2004)

Phylogeography of Trochodendron aralioides (Trochoden-

draceae) in Taiwan and adjacent areas. Journal of Biogeo-

graphy, 31, 12511259.

Hughes, S.J. & Malmqvist, B. (2005) Atlantic Island freshwater

ecosystems: challenges and considerations following the

EU Water Framework Directive. Hydrobiologia, 544,

289297.

Johnson, K.P., Adler, F.R. & Cherry, J.L. (2000) Genetic and

phylogenetic consequences of island biogeography. Evolu-

tion, 54, 389396.

Kim, J.-W. (1988) The phytosociology of forest vegetation on

Ulreung-do, Korea. Phytocoenologia, 16, 259281.

Lande, R. (1992) Neutral theory of quantitative genetic vari-

ation in an island model with local extinction and colon-

ization. Evolution, 46, 381389.

Lawrence, S.R., Johnson, M., Tubb, S.R. & Marshallsea, S.J.

(1999) Tectono-stratigraphic evolution of the North Falk-

land region. Geological Society Special Publication, 153, 409

424.

MacArthur, R.H. & Wilson, E.O. (1967) The theory of island

biogeography. Princeton University Press, Princeton.

Marticorena, C., Stuessy, T.F. & Baeza, C.M. (1998) Catalogue

of the vascular flora of the Robinson Crusoe or Juan Fer-

nandez Islands, Chile. Gayana Botanica, 55, 187211.

McDougall, I. & Ollier, C.D. (1982) Potassium-argon ages

from Tristan da Cunha, South Atlantic. Geological Magazine,

119, 8793.

Miller, J.A. (1964) Age determinations made on samples of

basalt from the Tristan da Cunha group and other parts of

the mid-Atlantic Ridge. Philosophical Transactions of the

Royal Society of London Series B, 249, 565569.

Moore, D.M. (1968) The vascular flora of the Falkland islands.

British Antarctic Survey Scientific Report No. 60. British

Antarctic Survey, London.

Muellner, A.N., Tremetsberger, K., Stuessy, T.F. & Baeza, C.M.

(2005) Pleistocene refugia and recolonization routes in the

Southern Andes: insights from Hypochaeris palustris De

Wild (Asteraceae, Lactuceae). Molecular Ecology, 14, 203

212.

Ono, M. & Okutomi, K. (eds) (1985). Endemic species and

vegetation of the Bonin islands. AbocSha Co., Tokyo.

Perry, R. (1984) Galapagos. Pergamon Press, Oxford.

Pfosser, M., Guzy-Wrobelska, J., Sun, B.-Y., Stuessy, T.F.,

Sugawara, T. & Fujii, N. (2002) The origin of species of Acer

(Sapindaceae) endemic to Ullung Island, Korea. Systematic

Botany, 27, 351367.

Pfosser, M., Jakubowsky, G., Schluter, P.M., Fer, T., Kato, H.,

Stuessy, T.F. & Sun, B.-Y. (2005) Evolution of Dystaenia

takesimana (Apiaceae), endemic to Ullung Island, Korea.

Plant Systematics and Evolution, 256, 159170.

Pfosser, M., Stuessy, T.F., Sun, B.-Y., Jang, C.-G., Guo, Y.-P.,

Taejin, K., Hwan, K.C., Kato, H. & Sugawara, T. (in press)

Phylogeny of Hepatica (Ranunculaceae) and origin of

Hepatica maxima Nakai endemic to Ullung Island, Korea.

Biological Journal of the Linnean Society, in press.

Press, J.R. & Short, M.J. (eds) (1994). Flora of Madeira. The

Natural History Museum, London.

Roux, J.P., Ryan, P.G., Milton, S.J. & Moloney, C.L. (1992)

Vegetation and checklist of Inaccessible Island, central South

Atlantic Ocean, with notes on Nightingale Island. Bothalia,

22, 93109.

Rundle, H.D., Mooers, A.. & Whitlock, M.C. (1998) Single

founder-flush events and the evolution of reproductive

isolation. Evolution, 52, 18501855.

Santos, A. (1998) Orgen y evolucion de la flora Canaria. Ec-

ologa y cultura en Canarias (ed. by J.M. Fernandez-Palacios,

J.J. Bacallado and J.A. Belmonte), pp. 107129. Organismo

Autonomo: Complejo Insular de Museos y Centros, La

Laguna.

Schluter, D. (2000) The ecology of adaptive radiation. Oxford

University Press, Oxford.

Schneider, S., Roessli, D. & Excoffier, L. (2000) Arlequin ver.

2.000: a software for population genetics data analysis.

Genetics and Biometry Laboratory, University of Geneva,

Geneva.

Skottsberg, C. (1953) The vegetation of the Juan Fernandez

Islands. The natural history of Juan Fernandez and Easter

Island (ed. by C. Skottsberg), pp. 793960. Almqvist &

Wiksells, Uppsala.

Stuessy, T.F. & Ono, M. (eds) (1998) Evolution and speciation

of island plants. Cambridge University Press, Cambridge.

Stuessy, T.F., Foland, K.A., Sutter, J.F., Sanders, R.W. & Silva,

O.M. (1984) Botanical and geological significance of po-

tassium-argon dates from the Juan Fernandez Islands. Sci-

ence, 225, 4951.

Stuessy, T.F., Crawford, D.J. & Marticorena, C. (1990) Patterns

of phylogeny in the endemic vascular flora of the Juan

Fernandez Islands, Chile. Systematic Botany, 15, 338346.

Stuessy, T.F., Greimler, J. & Dirnbock, T. (2005) Landscape

modification and impact on specific and genetic diversity in

oceanic islands. Plant diversity and complexity patterns: local,

regional and global dimensions (ed. by H. Balslev and I.

Friis), pp. 89101. The Royal Danish Academy of Sciences

and Letters, Copenhagen.

Sun, B.-Y. & Stuessy, T.F. (1998) Preliminary observations on

the evolution of endemic angiosperms of Ullung Island,

Korea. Evolution and speciation of island plants (ed. by T.F.

Stuessy and M. Ono), pp. 181202. Cambridge University

Press, Cambridge.

Sun, B.-Y., Park, J.H., Kim, C.H. & Kim, K.S. (1997) Mor-

phological divergence of the genus Dystaenia (Apiaceae).

Korean Journal of Plant Taxonomy, 27, 481490.

Takayama, K., Ohi-Toma, T., Kudoh, H. & Kato, H. (2005)

Origin and diversification of Hibiscus glaber, species en-

demic to the oceanic Bonin Islands, revealed by chloroplast

DNA polymorphism. Molecular Ecology, 14, 10591071.

Tremetsberger, K., Stuessy, T.F., Guo, Y.-P., Baeza, C.M.,

Weiss, H. & Samuel, R.M. (2003) Amplified fragment length

polymorphism (AFLP) variation within and among popu-

lations of Hypochaeris acaulis (Asteraceae) of Andean

southern South America. Taxon, 52, 237245.

T. F. Stuessy et al.

1264 Journal of Biogeography 33, 12591265 2006 The Authors. Journal compilation 2006 Blackwell Publishing Ltd

Tremetsberger, K., Talavera, S., Stuessy, T.F., Ortiz, M.A.,

Weiss-Schneeweiss, H. & Kadlec, G. (2004) Relationship of

Hypochaeris salzmanniana (Asteraceae, Lactuceae), an

endangered species of the Iberian Peninsula, to H. radicata

and H. glabra and biogeographical implications. Botanical

Journal of the Linnean Society, 146, 7995.

Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T.,

Hornes, M., Fritjers, A., Pot, J., Peleman, J., Kuiper, M. &

Zabeau, M. (1995) AFLP: a new technique for DNA

fingerprinting. Nucleic Acids Research, 23, 44074414.

Wace, N.M. (1961) The vegetation of Gough Island. Ecological

Monographs, 31, 337367.

Wace, N.M. & Holdgate, M.W. (1958) The vegetation of Tri-

stan da Cunha. Journal of Ecology, 46, 593620.

Wagner, W.L. & Funk, V.A. (eds) (1995). Hawaiian biogeo-

graphy: evolution on a hot spot archipelago. Smithsonian

Institution Press, Washington, D.C.

Wagner, W.L., Herbst, D.R. & Sohmer, S.H. (1999) Manual of

the flowering plants of Hawaii, Vol. 1, 2nd edn. University of

Hawaii and Bishop Museum Press, Honolulu.

Wendel, J.F. & Percival, A.E. (1990) Molecular divergence in

the Galapagos IslandsBaja California species pair, Gossy-

pium klotschianum and G. davidsonii (Malvaceae). Plant

Systematics and Evolution, 171, 99115.

Wiggins, I.L. & Porter, D.M. (1971) Flora of the Galapagos

islands. Stanford University Press, Stanford.

Wildpret de la Torre, W. & Del Arco Aguilar, M. (1987)

Espana Insular, II: Las Canarias. La Vegetacion de Espana

(ed. by M. Peinado Lorca and S. Rivas-Martnez), pp. 517

542. Universidad Alcala de Henares, Alcala de Henares.

Wills-Johnson, M.K., King, M., Campbell, H., Atkinson, I.,

Schiel, D., Richards, R., Given, D., Dugdale, J. Emberson, R.,

Bell, B., Millener, P. & Munn, A. (1996) The Chatham is-

lands: heritage and conservation. Canterbury University

Press, Christchurch.

Woo, H.-K., Kim, J.-H., Yeau, S.-H. & Lee, N.S. (2002)

Morphological and isozyme divergence in Korean Hepatica

sensu stricto (Ranunculaceae). Plant Systematics and Evo-

lution, 236, 3344.

BIOSKETCH

Tod Stuessy is Professor and Head of the Department of

Systematic and Evolutionary Botany, and Director of the

Botanical Garden, Institute of Botany, University of Vienna.

His general research interests are in island biology, evolu-

tion of the flora of southern South America, principles and

methods of classification, and systematics of Asteraceae. His

recent research focuses on patterns of genetic variation

within the Juan Fernandez (Robinson Crusoe) archipelago,

phylogeny and character evolution within the ancient

complex of Asteraceae (Barnadesioideae), and phylogenetic,

populational and biogeographic studies in Hypochaeris

(Asteraceae, Lactuceae) of Andean and southern South

America.

Editor: Jose Mara Fernandez-Palacios



Documents

Anagenetic Evolution in Island Plants