Adaptive Radiation and Genetic Differentiation in the Hawaiian Silversword

Alliance (Compositae: Madiinae)

Martha S. Witter; Gerald D. Carr

Evolution, Vol. 42, No. 6. (Nov., 1988), pp. 1278-1287.

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Evolution, 42(6), 1988, pp. 1278-1287

ADAPTIVE RADIATION AND GENETIC DIFFERENTIATION IN THE

HAWAIIAN SILVERSWORD ALLIANCE (COMPOSITAE: MADIINAE)

MARTHAS. WITTER
Laboratory of Biomedical and Environmental Sciences, University of California,
Los Angeles, CA 90024
AND

GERALDD. CARR
Department of Botany, University of Hawaii, Honolulu, HI 96822

Abstract. -The Hawaiian silversword alliance consists ofthe three genera Dubautia, Argyroxiphium,
and Wilkesia, and is a classic example of adaptive radiation in an insular setting. Genetic variation
and interspecific genetic differentiation based on ten enzyme loci are described for Dubautia and
Wilkesia. Genetic identities among species span the range of values expected from interpopulation
c_omparisons within a single species ( I = 0.90-1.00) to those typical of interspecific comparisons
( I = 0.67). Genetic-identity values correspond to biogeographic distribution and morphological
distinctiveness, supporting a correlation of increasing genetic distance associated with the time of
separation among lineages. It may be inferred that the high genetic identities observed within the
Hawaiian Madiinae and other island plant groups are due to limited time spans available for taxa
to accumulate new genetic variation through mutation. It appears that species may remain genet-
ically similar ( I > 0.90) even after time spans on the order of magnitude of 1,000,000 years.

Received June 2, 1987. Accepted March 30, 1988

The Hawaiian silversword alliance (Com-
positae: Madiinae) consists of 28 species in
three endemic genera: Argyroxiphium, Du-
bautia, and Wilkesia. It is one of the classic
examples of a group of organisms that have
undergone adaptive radiation in an insular
setting (e.g., Carlquist, 1965). Members of
the silversword alliance can be found in
nearly all habitat types within the Hawaiian
Islands, and the range of morphological
variation includes rosette plants, trees,
shrubs, subshrubs, and a vine (Carr, 1985;
Fig. 1).
The eight major islands of the Hawaiian
chain are volcanic in origin. They extend
for 400 miles in a linear age progression:
Kauai is approximately 6,000,000 years old,
while Hawaii has been in existence for less
than 500,000 years (MacDonald et al.,
1983). This relatively simple geologic his-
tory provides a clear framework for the bio-
geographic history of Hawaiian organisms
and greatly facilitates inferences concerning
the evolutionary processes involved in the
origin ofunique Hawaiian species (e.g., Car-
son and Kaneshiro, 1976; Ganders and Na-
gata, 1984).
In the case of the Hawaiian Madiinae,
cytological and biosystematic data suggest
that the modern distribution of the Hawai-
ian Madiinae is best explained by an origin
on the island of Kauai. The primitive con-
dition in the group is a cytotype of 14 pairs
of chromosomes. All species of Wilkesia and
Argyroxiphium have 14 pairs of chromo-
somes, while Dubautia contains species with
a haploid chromosome number of either 13
or 14 (referred to hereafter as Dubautia n =
14 and Dubautia n = 13). Wilkesia and the
majority of the Dubautia n = 14 species are
single island endemics restricted to the is-
land of Kauai and are among the most mor-
phologically specialized and distinctive
species (Fig. 1). The Dubautia n = 13 species
are largely restricted to the youngest islands
and are all phylogenetically linked through
a single aneuploid reduction event to a mor-
phologically and distributionally unique
Dubautia n = 14 species, D. scabra (Carr,
1978; Carr and Kyhos, 198 1). Species found
down the island chain are ultimately the
result of dispersal from Kauai (Carr et al.,
1989). Thus, species with a haploid chro-
mosome number of 14 are presumed to rep-
resent the oldest lineages within the Hawai-
ian Madiinae, and those with n = 13 are
presumed to be the most recently evolved
taxa. The purpose of this paper is to present
the results of an electrophoretic analysis of
the Hawaiian Madiinae in order to examine
 ADAPTIVE RADIATION IN SILVERSWORDS

the degree of genetic differentiation and the

population-genetic structure associated with
WILKESIA n.14
adaptive radiation in this insular plant
KAUAl
group.
OAHU
*(2) -MAUI COMPLEX

MATERIALS AND METHODS O D

Of the 12 enzyme systems described for

the Hawaiian Madiinae (Witter, 1986), five
enzymes representing ten loci could be pos-
itively identified to be homologous among
all taxa, and allelic variation for these could
be accurately assigned to a particular locus.
The ten loci are: Pgi-c3, Pgi-c4, Got- 1, Got-
2, Tpi-1, Tpi-2, Tpi-3, Me, Idh-pl, and Idh-
DUBAUTIA n.14
c2. Two pairs of loci, Pgi-c3/Pgi-c4 and Tpi-
2/Tpi-3 behave as duplicate loci and were
interpreted to be the expression of divergent
loci in a polyploid genome (Witter, 1986).
The genetic basis of the observed isozyme
patterns was inferred from various lines of
evidence: analysis of hybrid progeny from DUBAUTIA n.13
interspecific crosses; patterns of interspe- 0

cific variation among species with fixed al-

lelic differences; conformance to Hardy-
Weinberg ratios within polymorphic species;
and conformance to published patterns of
enzyme expression in the Compositae and
other plant species, in terms of their sub-
cellular localization, subunit organization,
and the basic number of loci expected in the
absence of gene duplication or polyploidy.
A full description of the genetic basis of all
isozyme patterns is given in Witter (1986).
These loci are used to analyze genetic vari-
ation and genetic differentiation in the
Hawaiian Madiinae.
The enzymes were resolved as follows:
glutamate oxaloacetate transaminase (GOT)
and plastid isocitrate dehydrogenase (IDHp)
with 0.1 M Tris-6.9 mM citrate gel and 0.1
M sodlurn hydroxide-0.3 M borate electrode
buffer at pH 8.8; cytoplasmic isocitrate de-
hydrogenase (IDHc) and phosphoglucoiso-
merase (PGI) with a 0.9 M Tris-0.02 M
EDTA-0.5 M borate buffer at pH 8.6; malic
enzyme (ME) with a 0.13 M Tris-0.045 M
citrate buffer at pH 7.0; and triose phos-
phate isomerase (TPI) with 0.05 M Tris-
0.008 M citrate gel and 0.03 M lithium hy-
droxide-0.19 M borate electrode buffer. The
staining methods and the gel buffers are those
which have been widely used and detailed
procedures are described in Witter (1986).
FIG.1. Distribution and endemicity of the species
of the Hawaiian Madiinae within the Hawaiian Is-
lands.
All plant extracts were derived from mature
leaf tissue ground in liquid nitrogen with an
extract buffer composed of 0.05 M Tris, 0.0 1
M ascorbate, 0.006 M bisulfite, 0.012 M
DIECA, 0.002 M EDTA (Na,), 0.20 M su-
crose, 0.2% 2-mercaptoethanol, 5% PVP
(MW 40,000) at pH 7.3. The gels were 12.5%
horizontal starch gels (Sigma starch).
Eighteen species were examined electro-
phoretically. Collection localities are given
in Witter (1986). Each species was repre-
sented by 7-2 1 individuals (Table 1) from
which leaf material had been collected in
the field. The sampling scheme emphasized
interspecific comparisons in order to max-
imize the range of interspecific differences.
Both species of Wilkesia (100°/0), most of
the species of Dubautia n = 14 (83%), and
all of the species of Dubautia n = 13 (100%)
were sampled. Heterozygosity estimates and
genetic distances (Nei, 1972, 1978) were
calculated with allele frequencies using the
1280 M . S . W I T T E RAND G. D. CARR

TABLE1. Genetic variability in Dubautza and Wtlkesia, based on ten loci. Standard errors are i n parentheses.

A locus is considered to be polymorphic i f more than one allele is detected. The mean heterozygosity expected

is a biased estimate (Nei, 1978).

Mean sample slre Mean number of Percentage of l o c ~ Mean Hardy-Welnberg

Taxon (haplo~dchromosome number) per locus alleles per locus polymorphic expected heterozygoslty

Wilkesia hobdyi
( n = 14)
W . gymnoxiphium
( n = 14)
Dubautia laxa (Kauai)
( n = 14)
D. laxa (Waianae)
( n = 14)
D. paleata
( n = 14)
D. raillardioides
( n = 14)
D. plantaginea (Waianae)
( n = 14)
D. plantaginea (Koolau)
( n = 14)
D. knudsenii
( n = 14)
D. latfolia
( n = 14)
D. scabra leiophylla (Maui)
( n = 14)
D. s. scabra (Hawaii)
( n = 14)
D. ciliolata
( n = 13)
D. herbstobatae
( n = 13)
D. linearis hillebrandii
( n = 13)
D. sherjiana
( n = 13)
D. reticulata
( n = 13)
D. dolosa
( n = 13)
D. menziesii
( n = 13)
D. arborea
( n = 13)
D. platyphylla
( n = 13)

BIOSYS- I program of Swofford and Selan-
der (1981).
RESULTS
Genetic Variation
The mean expected heterozygosity for in-
dividual species of the Hawaiian Madiinae
is given in Table 1 . Allele frequencies for
all taxa are available from the senior author
upon request. All ten homologous loci ex-
hibit polymorphism in at least one species,
although three loci (Me, Idh-pl,and Idh-
c2) are monomorphic for a single allele in
the majority of species. The other seven loci
(70%) are polymorphic within some species
and may exhibit fixed interspecific allelic
differences. In all, 62 alleles have been ob-
served at these ten loci. Averaged over all
populations, the mean number of alleles per
 ADAPTIVE RADIATION IN SILVERSWORDS 1281

TABLE2. Genetic variation in the Hawaiian Madiinae and other relevant plant groups. Data are from the
following sources. Tetramolopium: Lowrey and Crawford (1985);Bidens: Sun (1986);Solanum (Lasiocarpa):
Whalen and Caruso (1983);Lisianthius: Sytsma and Schaal(1985); mainland average: Hamrick et al. (1979)and
Hamrick (1983).PTOT = frequency of all loci polymorphic in at least one taxon; P = frequency of polymorphic
loci per population; AL = averge number of alleles per locus per population; Ap = average number of alleles
per polymorphic locus; HET = mean expected heterozygosity per population averaged over all populations.

Plant group PTOT P AL AP HET

Island shrubs:
Hawaiian Madiinae 1 .OO 0.24 1.29 2.20 0.075
Tetramolopzum 0.27 0.07 1.09 2.13 <0.01
Bzdens 0.26 0.12 1.16 2.47 0.045
Tropical mainland shrubs:
Solanum (Lasiocarpa) 0.25 0.04 1.13 2.00 <0.01
Lisianthius
Lowland 0.67 0.23 1.23 2.00 0.059
Cloud forest - 0 1 .OO - 0
Mainland average - -0.40-0.50 - -3.0 0.14

locus is 1.29 (1.1-1.7), the mean number of
alleles per polymorphic locus is 2.20, the
average percentage of loci polymorphic per
population is 24.3 (10.0-40.0), and the mean
heterozygosity expected is 0.075 (0.0 13-
0.124). The mean heterozygosity expected
is similar for Wilkesia, Dubautia n = 14,
and Dubautia n = 13.
Genetic variation is not as low in popu-
lations of the Hawaiian Madiinae as it is in
other island plant groups that have been
measured. Compared to both Tetramolo-
pium and Bidens, the Hawaiian Madiinae
are more variable in all measures of genetic
variation (Table 2; Lowrey and Crawford,
1985; Sun, 1986). However, the Hawaiian
Madiinae have only half the level of genetic
variation observed in average mainland
populations (Table 2; Hamrick et al., 1979;
Hamrick, 1983).
Genetic Dlferentiation Between Species
A matrix of Nei's (1972) genetic-distance
and genetic-identity (I)values for all pair-
wise population comparisons is given in Ta-
ble 3. Critical values of genetic identity in
plant species have been reviewed by Gott-
lieb (198 1) and Crawford (1983). Conspe-
cific populations have a mean genetic iden-
tity of 0.95, with most plant species falling
in the range of 0.95-1.00, while the maxi-
mum range observed is 0.87-1.00. Inter-
specific comparisons in general produce
smaller values for I, with a mean of 0.67.
In comparison, some pairs of morphologi-
cally distinct species of the Hawaiian Ma-
diinae have very high genetic identities (0.95
or more), values characteristic of pairs of
populations rather than distinct species. The
two species of Wilkesia and some species
combinations within both chromosome
sections ofDubautia are this high. However,
substantial genetic differentiation has oc-
curred between some lineages, on the order
of magnitude expected for interspecific
comparisons.
Figure 2 illustrates the average degree of
genetic differentiation within and among
species of Wilkesia, Dubautia n = 14, Du-
bautia n = 13, and D. scabra. The greaier
morphological differentiation and diversity
pointed out by Carr (1978, 1985) in the
species of Dubautia n = 14 relative to species
of Dubautia n = 13 are paralleled by a great-
er average amount of allozymic differentia-
tion among Dubautia n = 14 taxa. Typical
levels of interspecific differentiation are
achieved only among the n = 14 species (1
= 0.69) originating on Kauai. The more re-
cently evolved Dubautia n = 13 species re-
main genetically similar (mean I = 0.95)
and have values close to those observed in
other island plant groups. Wilkesia is ge-
netically differentiated from Dubautia, but
some of the Dubautia n = 14 species are as
distinct from each other as the average
species of Dubautia is from Wilkesia. Du-
bautia latifolia, as well as having an unusual
life-form and being morphologically unique,
is distinctive genetically, at least as distinc-
tive from other species of Dubautia as is
Wilkesia gym noxiphium.
1282 M. S . W I T T E R A N D G. D. CARR

TABLE3. Matrix o f Nei's (1972)genetic-distance coefficients(below diagonal) and Nei's genetic-identity coef-

ficients (above diagonal) for the Hawaiian Madiinae.

Taxon
Taxon 1 2 3 4 5 6 7 8

1 ) Wilkesia hobdyi

2) W . gymnoxiphium

3) Dubautia laxa (Kauai)

4) D. laxa (Waianae)

5) D. paleata

6 ) D. raillardioides

7 ) D. plantaginea (Waianae)

8) D. plantaginea (Koolau)

9 ) D. knudsenii

10) D. latifolia
1 1 ) D. scabra leiophylla (Maui)
12) D. s. scabra-Maui
13) D. ciliolata
14) D. herbstobatae
15) D. linearis hillebrandii-Hawaii
16) D. s h e r f i n a
17) D. reticulata
18) D. dolosa
19) D. menziesii
20) D. arborea
2 1 ) D. platyphylla

For all polymorphic loci, there is a single morphic loci, and these frequently have
widespread allele that occurs in some species fewer alleles per locus (Table 2; Hamrick et
of Wilkesia, Dubautia n = 13, and Dubautia al., 1979). Tetramolopium and Bidens have
n = 14. Some species may be polymorphic low levels of genetic variability because
for the common allele and a variant, while species in both genera have a large number
other species may be fixed for a unique vari- of identical monomorphic loci (Table 2;
ant. The low genetic identities observed be- Lowrey and Crawford, 1985; Sun, 1986). In
tween the n = 14 species on Kauai are due Tetramolopium, even variable loci are still
to an increase in the number of polymor- monomorphic in many populations. Den-
phisms with unique alleles and a greater droseris similarly has highly monomorphic
number of fixed unique alleles. populations (Crawford et al., 1985b; Craw-
Species pairs that have been hypothesized ford, pers. comm.). While populations of
to be closely related and that share one or the Hawaiian Madiinae are not as extremely
more unique alleles (with the number of monomorphic, genetic variation is only
shared unique alleles and the average ge- about halfthat expected in mainland species
netic identity between species pairs) are: D. (Table 2).
paleata and D. raillardioides (I, I = 0.786), To explain low genetic variation in island
D. knudsenii and D. paucijlorula (2, incom- populations, it is necessary to explain the
plete data for the calculation of Z), D. sherf- lack of multiple alleles at any locus. Among
jiana and D. herbstobatae (1, I = 0.89), D. the stochastic factors influencing levels of
reticulata and D. dolosa (3, I = 0.997), D. genetic variation, the frequency and size of
menziesii, D. platyphylla, D. arborea, and bottleneck events will be of major impor-
D. ciliolata (3, f = 0.962). tance (Nei et al., 1975).
All island populations have experienced
founder effects with genetic bottlenecks dur-
DISCUSSION ing the process of their initial colonization
Genetic Variation in Island Taxa following long-distance dispersal. Within
Island plant populations are less variable Hawaii or any island archipelago, many
genetically than typical mainland popula- populations experience additional founder
tions; island populations have fewer poly- effects as they migrate down the island chain
 ADAPTIVE RADIATION IN SILVERSWORDS 1283

TABLE3. Extended.

or between isolated habitats within an is- Reduced genetic variability may not
land. The genetic consequences of founder characterize all island plant groups. Species
events have been documented for popula- that are the products of adaptive radiation
tions known to have originated in historical are generally discrete, isolated species. They
times by long-distance dispersal of relative- represent only one end of the spectrum of
ly few individuals. These populations have variation and population structure ob-
decreased levels of genetic variation, caused
by the loss of alleles following long-distance
dispersal (Schwaegerle and Schaal, 1979;
Marshall and Weiss, 1982;Clegg and Brown,
1983; Levin, 1984). This is also illustrated
by several populations of the Hawaiian Ma-
diinae on younger islands that have lost al-
leles present in polymorphic populations on
older islands (e.g., D. laxa [Tpi-I and Tpi-
21, D. linearis [Per-31).
I
DUBAUTIA n=14
6SPECIES
I

Island populations frequently have re-

stricted distributions and relatively small -I= 0.894
population sizes, conditions unde; which
-1= 0.795
(0.67. 0.95) (0.77- 0.99)
genetic drift is likely to occur. Population
size may be one of the most significant fac-
tors relating to the differences observed in 1 SUBSPECIES

the level ofgenetic variability of the Hawai-

ian Madiinae compared to that of Tetra-
molopium and Dendroseris. Many species FIG.2. Summary of interspecific genetic identities
of the ~ ~~ ~ ~dare iabundant,
~i ~ ~ i(Nei, ~1978)i within and~between Wilkesia
~ species, Du-
bautia n = 14 species, Dubautia n = 13 species, and
dominant species in their 'Om- Dubautia scabra. Irepresents the average of all pairwise
munities, while Tetramolo~iumand Den- comparisons within or between species groups. The
droseris have much smaller populations with range of the pairwise comparisons corresponding to
highly localized distributions. each mean is given in parentheses.
1284 M. S. WITTER AND G. D. CARR

served in island ecosystems. Long-lived pe- of as a process involving two overlapping

rennials with large population sizes, such as stages: the first is the divergence in gene
the dominant Hawaiian forest trees Acacia frequencies shared due to common ances-
koa and Metrosiderospolymorpha are likely trv. ., and the second is the accumulation of
to have higher levels of genetic variability newly arisen mutations among independent
(Loveless and Hamrick, 1984). These tree lineages. The second process, whereby new
species could also provide a valuable model mutations are fixed, is presumably the slow-
for assessing the effects of founder events er process and the one that becomes im-
and population size on levels ofgenetic vari- portant between more distantly related taxa
ability. (Baverstock et al., 1979).
The process by which island species come
Genetic Diferentiation in Island Taxa to differ genetically from each other in terms
The Hawaiian Madiinae have some ex- of allozyme variation is demonstrably dif-
tremely high interspecific genetic identities, ferent than that of polymorphic mainland
similar to those reported in other island plant populations in the early stages of diver-
groups (Tetramolopium in Hawaii [Lowrey gence. The Hawaiian Madiinae graphically
and Crawford, 19851; Dendroseris in the illustrate that the mutation process, rather
Juan Fernandez Islands [Crawford et al., than shifts in existing gene frequencies, lim-
1985bl; and Bidens in Hawaii [Helenurm its the rate at which gene differentiation oc-
and Ganders, 1985; Sun, 19861). Outside of curs between species with limited genetic
islands, the only other examples of high ge- variability. Within the Hawaiian Madiinae.
netic identities are found between recently very few species share a large pool of com-
diverged species, or those with recent pro- mon polymorphisms by which genetic dif-
genitor-derivative relationships (Gottlieb, ferentiation could be achieved through the
1973, 1974; Gottlieb and Pilz, 1976; Craw- fixation of alternative alleles from a com-
ford and Smith, 1982; Soltis, 1982, 1985; mon polymorphism. Most species of Du-
Gottliebet al., 1985; Crawfordet al., 1 9 8 5 ~ ; bautia n = 13 on Maui and Hawaii share a
Ranker and Schnabel, 1986). common allele at most loci. Genetic differ-
The high interspecific genetic identities entiation can therefore occur only as new
observed in island populations of conge- mutations arise in separate lineages and be-
neric plant species have been proposed to come fixed. The modern allele distribution
be the result of introductions coupled with in the n = 14 species supports a similar
founder events, which reduced the amount process in their evolutionary past. The scat-
of genetic variation in populations; because tered presence of a single allele suggests a
these introductions were recent, the amount common ancestral lineage, but the large
of time available has been insufficient for number of unique alleles, restricted to single
new variation to accumulate in various lin- species or closely related species, suggests
eages (e.g., Crawford et al., 1985b). The that the novel alleles arose inde~endentlv
Hawaiian Madiinae offer an exceptionally and subsequent to separation of the differ-
clear illustration that allozymic divergence ent n = 14 lineages.
among genetically depauperate taxa does In contrast to island populations, where
depend on the slow accumulation of new divergence is dependent on the origin and
genetic variation. fixation of new mutations, mainland pop-
In general, it is the presence of loci with ulations in the early stages of genetic differ-
fixed allele differences among species that entiation diverge through changes in poly-
accounts for the usual range of observed morphic gene frequencies. Shifts in gene
interspecific genetic distances (Ayala, 1975). frequencies can be seen clearly in the initial
This means that species are usually either genetic differentiation of genetically vari-
identical or completely divergent at indi- able mainland populations resulting from
vidual loci ( I = 1 .OO or I = O), and it is the either allopatric separation or in species re-
number of loci that remain identical or have lated as progenitor and derivative. Species
diverged that affects the overall interspecific of Layia (Warwick and Gottlieb, 1985),
distance value. The accumulation of genetic Limnanthes (Kesseli and Jain, 1984), and
differences between species can be thought two varieties of Coreopsis cyclocarpa (Craw-
 ADAPTIVE RADIATION IN SILVERSWORDS
ford and Bayer, 198 1) all illustrate the pre-
dominant effect of existing genetic variation
on genetic divergence. For example, diver-
gence between the varieties of Coreopsis cy-
clocarpa was due to divergence in allele fre-
quencies at 18 of 20 loci, with 14 unique,
generally low-frequency alleles present in
one variety and four present in the other.
Species-groups characterized by this pattern
of genetic differentiation all have relatively
large populations with high levels of genetic
variability (25-50% polymorphic loci/pop-
ulation and 2.5-3.4 alleles/polymorphic lo-
cus).
The pattern of genetic differentiation ob-
served in island taxa is not a characteristic
of organisms in island ecosystems per se but
is a function of their history and population
structure. Slow genetic divergence based on
the accumulation of mutations could be ex-
pected in any group with a population struc-
ture similar to that of typical island taxa.
Lisianthius and Solanum are genera of pe-
rennial tropical shrubs with relatively small,
isolated populations, analogous to those of
many island species. Levels of genetic vari-
ation are very similar between the island
and mainland plant groups (Table 2). In-
terspecific comparisons in Lisianthius and
Solanum show reduced genetic identities (I
< 0.67; Whalen and Caruso, 1983; Sytsma
and Schaal, 1 9 8 5 ~which
)~ are presumably
due to longer periods of isolation than those
for island species only several million years
old (Whalen and Caruso, 1983). The allele
distribution among taxa in both Solanum
and Lisianthius suggests that genetic differ-
ences among species must have originated
to a large degree from the origin and fixation
of new variation in separate lineages. In the
derivative cloud-forest populations of Lisi-
anthius skinneri only two of 15 alleles pres-
ent in the ancestral lowland populations were
absent, while 14 of 26 alleles present in the
cloud-forest taxa were unique (Sytsma and
Schaal, 1985a, 1985b). This pattern suggests
that drift of ancestral frequencies is unlikely
and that genetic divergence in these genet-
ically depauperate tropical shrubs is also a
mutation-dependent process.
The rate at which populations diverge may
be different, depending on whether the ini-
tial stages of genetic differentiation are gov-
erned by mutation or divergence in ances-
1285
tral frequencies. Application of the term
"recent" to species with high genetic iden-
tities may have very different meanings de-
pending on the initial levels of genetic vari-
ation in ancestral populations and the
subsequent process of genetic differentia-
tion. When the concept of "recent" species
has been coupled to an absolute time scale,
it usually corresponds to species origins less
than 10,000-20,000 years B.P.(e.g., Lewis,
1973; Crawford et al., 1 9 8 5 ~Lowrey
; and
Crawford, 1985; Stebbins, 1982). The most
recent species of the silversword complex
can be used as a model for the time nec-
essary to accumulate typical levels of inter-
specific gene differences in genetically de-
pauperate species by making the assumption
that the age of the islands to which the
species are endemic represents an upper age
boundary. The results for species of Dubau-
tia n = 13 indicate that species could be on
the order of 500,000-1.5 million years old
and still possess the very high genetic iden-
tities characteristic of "recent" mainland
progenitor-derivative species pairs. Within
Dubautia, it is only in the lineages that have
originated on Kauai that the degree of ge-
netic differentiation typical of interspecific
comparisons is approached. Within the time
frame of the age of Kauai, this corresponds
maximally to species ages of 5-6 million
years.
The extremely high genetic identities in
Tetramolopium are actually quite compa-
rable to the species of Dubautia with the
same biogeographic history, i.e., the n = 13
species that have originated on the recent
islands of Hawaii and Maui and have been
dispersed from there. The isozyme data
alone do not support an origin more recent
than 20,000 years B.P.for Hawaiian species
of Tetramolopium, although this idea is
based largely on the age of particular habitat
types (Lowrey, 198 1; Lowrey and Crawford,
1985). Bidens is similar to the Hawaiian
Madiinae in that species have originated on
Kauai and dispersed down the chain from
there (F. R. Ganders, pers. comm.). The
genus therefore includes taxa that presum-
ably predate the origin of Maui or Hawaii.
Unfortunately, Bidens cosmoides, the species
most comparable to the Kauai endemics of
Dubautia, has not been examined electro-
phoretically. It is therefore not clear wheth-
1286 M. S. WITTER AND G. D. CARR
er this species of Bidens follows the same
pattern of increased genetic differentiation
as the Hawaiian Madiinae on Kauai. There
is a close parallel between the biogeographic
pattern of genetic divergence observed in
the Hawaiian Madiinae and that found in
the Hawaiian Drosophila (Sene and Carson,
1977; Cam et al., 1989).
It is the recency of many island taxa, cou-
pled with low levels of genetic variability as
a result of founder effects and population
structure, that promotes a pattern of high
interspecific genetic identities, so different
from that observed in most mainland plant
groups. The significance of mutation in the
genetic differentiation of island populations
suggests that the sampling scheme in this
survey, which is based on low numbers of
individuals/species and few interpopulation
comparisons, has some serious drawbacks.
The inability to detect low-frequency alleles
if they are present, while having a minimal
effect on the quantitative estimate of genetic
identities, profoundly influences the inter-
pretation of allelic differentiation among
taxa and conclusions regarding the origin of
genetic differences between species.
ACKNOWLEDGMENTS
This work was supported partially by NSF
Grant DEB-78228 19 to G.D.C., by the De-
partment of Botany of the University of Ha-
waii, by the Pacific Tropical Botanic Gar-
den, and by the Office of Health and
Environmental Research of the U.S. De-
partment of Energy. The authors thank L.
D. Gottlieb for assistance in resolving sev-
eral of the enzyme systems, J. Wendel for
discussions of extraction methods, D. Buth
and D. Herman for providing and assisting
with the computer program, P. W. Rundel
for general and technical support, and R.
Olmstead and two anonymous reviewers for
helpful comments on the manuscript.
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Corresponding Editor: J. L. Hamrick