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Botanical Journal of the Linnean Society, 2014, 174, 289–304. With 3 figures
Do the island biogeography predictions of MacArthur
and Wilson hold when examining genetic diversity on
the near mainland California Channel Islands?
Examples from endemic Acmispon (Fabaceae)
MITCHELL E. MCGLAUGHLIN1*, LISA E. WALLACE2, GREGORY L. WHEELER2,
GERALD BRESOWAR1, LYNN RILEY3, NICHOLAS R. BRITTEN3 and
KAIUS HELENURM3
1
School of Biological Sciences, University of Northern Colorado, Greeley, CO 80639, USA
Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762, USA
3
Department of Biology, University of South Dakota, Vermillion, SD 57069, USA
2
Received 19 April 2013; revised 27 August 2013; accepted for publication 10 September 2013
The California Channel Islands are a group of eight oceanic islands located off the coast of southern California that
are substantially closer to the mainland than most other well-studied island systems. The equilibrium theory of
island biogeography proposed by MacArthur and Wilson posits that species diversity on an island will be positively
impacted by island area and negatively impacted by isolation, which has been confirmed for the Channel Islands.
In this study, we have extended MacArthur and Wilson’s theory to examine how levels of genetic diversity relate
to four island characteristics (island area, distance to the mainland, distance to the nearest island, plant diversity)
in the endemic perennial taxa of Acmispon (Fabaceae) on the Channel Islands. We sampled two island species of
Acmispon, A. argophyllus and A. dendroideus, from all islands, and mainland sister taxa for nuclear microsatellites, low-copy nuclear sequence and plastid sequence data. We found that only one measure of diversity from one
genetic region (low-copy nuclear) was correlated with island area, that there was no support for a relationship
between genetic diversity and distance to the mainland and that distance to the nearest island was a predictor of
low-copy nuclear genetic diversity. Plant diversity was a significant predictor of plastid genetic diversity when
considering all samples. We conclude that the equilibrium theory of island biogeography does not hold for measures
of genetic diversity in the Channel Island endemic Acmispon based on island area and distance to the mainland.
The short distance between individual islands and the mainland probably facilitates a moderate rate of mainland
to island dispersal, preventing the islands from functioning as isolated biogeographic units. © 2013 The Linnean
Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304.
ADDITIONAL KEYWORDS: chloroplast DNA – colonization – DNA sequence data – genetics –
microsatellites.
INTRODUCTION
Publication of The Theory of Island Biogeography
(MacArthur & Wilson, 1967) represents one of the
defining theoretical contributions to the field of biogeography and a foundation of modern understanding
of evolutionary patterns on oceanic islands. In this
work, MacArthur and Wilson proposed the equilib*Corresponding author. E-mail:
[email protected]
rium theory of island biogeography, which postulates
that ‘the number of species on a given island is
usually approximately related to the area of the
island . . .’ (MacArthur & Wilson, 1967: 17). Equilibrium is achieved by a balance between immigration
and extinction regulated primarily by island area,
which also correlates with environmental diversity
and, to a lesser degree, island isolation (Simberloff,
1974). The island area–species diversity relationship
has been documented on many oceanic islands
(reviewed in Schoenherr, Feldmeth & Emerson, 2010)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
289
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M. E. MCGLAUGHLIN ET AL.
and extended to islands of habitat in continental
systems (e.g. White, Miller & Ramseur, 1984; Watling
& Donnelly, 2006).
Over time, the equilibrium theory of island biogeography has been applied to other island diversity relationships (reviewed in Losos, Ricklefs & MacArthur,
2009), such as correlations between island area and
genetic diversity (Johnson, Adler & Cherry, 2000) or
species diversity and genetic diversity (Vellend, 2003,
2005; Vellend & Orrock, 2009), as addressed here. As
genetic diversity in populations is a product of both the
diversity contained in immigrants (both the initial
founders and subsequent dispersers) and population
size, island area and isolation should have a large
and consistent impact on levels of genetic diversity.
Johnson et al. (2000) proposed a theoretical model to
predict rates of migration and extinction of island
organisms based on population genetic data, which
focused largely on the amount of divergence between
island and mainland populations, although island size
and island isolation were identified as major determinants of genetic diversity. In a similar vein, Vellend
(2003) proposed the species–genetic diversity correlation (SGDC), which suggests that there is a correlation
between species diversity and genetic diversity in
island systems, and that SGDC should be highest on
large islands close to a mainland source. The SGDC
model is interesting because it is based on the relationship between the number of species on an island
and the genetic diversity of a single taxon or a small
number of focal taxa. Because of the well-established
island area–species diversity relationship, the SGDC
model serves as a theoretical and empirical bridge for
thinking about the impacts of island area, island
isolation and species diversity on genetic diversity
contained within island taxa.
Despite theoretical predictions that island characteristics should be correlated with levels of genetic
diversity in island populations, few studies have
empirically tested these relationships, particularly in
plants. Yamada & Maki (2012) found a significant
negative correlation between genetic diversity and
distance to the mainland, but no relationship between
diversity and island area in Weigela coraeensis
Thunb. (Caprifoliaceae) from mainland Japan and
the Izu Islands. Inoue & Kawahara (1990) observed
a similar relationship between genetic diversity and
distance to the mainland in Campanula punctata
Lam. (Campanulaceae) from the Izu Islands, but no
statistical tests were performed. Vellend (2003, 2005)
took a broad approach to the relationship between
island characteristics and genetic diversity, demonstrating SGDC through empirical (Vellend, 2003) and
theoretical (Vellend, 2005) studies and that the relationship is strongly impacted by island area, island
isolation and environmental heterogeneity (only
addressed in Vellend, 2005). Although these studies
demonstrate that island characteristics can have a
significant impact on genetic diversity, this remains
an understudied area.
A commonly observed and tested relationship is
that island populations generally contain less genetic
diversity than their continental relatives (DeJoode &
Wendel, 1992; Frankham, 1997; Franks, 2010). The
relative lack of diversity on islands is attributed to
population establishment by a small number of founders, smaller population sizes and a higher probability of population extinctions on islands (Barton &
Charlesworth, 1984; Frankham, 1997). This relationship has been confirmed in multiple island systems
(e.g. Chung et al., 2004; Yamada & Maki, 2012), but
studies have generally been biased towards islands
that are closer to the mainland, attributable to use of
species that occur on both islands and mainland or
ease of identifying mainland sister taxa. In more
isolated island systems, levels of genetic diversity are
frequently compared with summary measures of
plant genetic diversity based on life history traits (e.g.
Hamrick & Godt, 1990; Hamrick et al., 1991). In such
studies, lower than average levels of genetic diversity have been found among plants on the Juan
Fernández Archipelago (Crawford et al., 2001),
Canary Islands (Francisco-Ortega et al., 2000),
Hawaiian Islands (DeJoode & Wendel, 1992) and
Bonin Islands (Ito, Soejima & Ono, 1998).
Although there are considerable data that suggest
that island plants contain less genetic diversity than
mainland species (Frankham, 1997), there are a
growing number of studies that have found that this
is not an absolute rule. For example, multiple studies
with Macaronesian plants (Fernández-Mazuecos &
Vargas, 2011; Desamore et al., 2012) have found more
diversity in island than mainland populations. Additional recent studies have failed to demonstrate clear
differences in the level of genetic diversity between
mainland and island populations (Su, Wang & Deng,
2010; García-Verdugo et al., 2013). Taken together,
these studies indicate that not all island species show
lower levels of genetic diversity than mainland relatives and that island age, isolation and historical
climatic patterns may have been important predictors
of genetic diversity.
The California Channel Islands are a group of
eight oceanic islands located off the coast of southern
California (Fig. 1) that have been the focus of several
botanical island biogeographic studies (Raven, 1967;
Thorne, 1969; Moody, 2000). Moody (2000) established a significant positive relationship between
island area and species diversity for endemic, native
and exotic plants on the Channel Islands and a
significant negative correlation between distance to
the mainland and native species richness, confirming
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
San Miguel
291
Santa Cruz
Anacapa
Los Angeles
Santa Rosa
Santa Catalina
Santa Barbara
San Nicolas
San Clemente
0
37.5
75
150 Kilometers
Sources: Esri, USGS, NOAA
Figure 1. Map of sampled populations of Acmispon from the California Channel Islands and southern California
mainland. Island A. argophyllus is indicated by circles: var. niveus (black), var. argenteus (white) and var. adsurgens
(grey). Acmispon dendroideus is indicated by squares: var. traskiae (black), var. dendroideus (white) and var. veatchii
(grey). Mainland populations of A. argophyllus var. argophyllus are indicated by black hexagons. The mainland population
of A. argophyllus var. fremontii is located approximately 660 km north of Los Angeles (not shown). Mainland A. glaber are
indicated by black stars. All population locations are approximate.
that degree of isolation is a barrier to colonization.
Furthermore, when island size and island isolation
are taken together, it is clear that island size is the
more significant predictor of native species diversity
(Moody, 2000). Thus, when considered in its entirety,
the flora of the California Channel Islands follows
the expectations of the equilibrium theory of island
biogeography.
Numerous genetic studies have investigated levels
of diversity in Channel Island endemic plants, generally with a conservation focus. Helenurm and colleagues (Helenurm, 2001, 2003; Dodd & Helenurm,
2002; Helenurm & Hall, 2005; Helenurm, West &
Burckhalter, 2005; Furches, Wallace & Helenurm,
2009; Riley, McGlaughlin & Helenurm, 2010) have
been conducting conservation genetic studies on
many of the endemic species on San Clemente. These
studies have generally found low levels of genetic
diversity, particularly in short-lived species, when
sampling only populations from San Clemente
(Helenurm, 2003; Helenurm & Hall, 2005; Helenurm
et al., 2005; Furches et al., 2009; Riley et al., 2010),
but the lack of diversity is probably attributable to
the rare and endangered status of sampled species; at
least one endemic species does not follow this pattern
(Helenurm, 2001). A limited number of studies have
investigated the genetics of Channel Islands plants
with multi-island distributions, generally identifying
low levels of diversity within and strong divergence
among islands (Bushakra et al., 1999; Wallace &
Helenurm, 2009) when sampling plants from two
islands. To date, no genetic studies have been published examining diversity and divergence in plants
distributed throughout the Channel Islands.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
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M. E. MCGLAUGHLIN ET AL.
Acmispon Raf. subgenus Syrmatium Vogel is an
ideal system for studying biogeographic patterns on
the Channel Islands. Two perennial Acmispon spp.,
A. argophyllus (A.Gray) Brouillet and A. dendroideus
(Greene) Brouillet, contain island-endemic varieties
that exhibit clear geographical structuring (Isley,
1981; Brouillet, 2008; Brouillet, 2013). Molecular phylogenetic studies have established that A. agrophyllus
and A. dendroideus are not sister taxa, but are closely
related (Allan & Porter, 2000). Liston, Rieseberg &
Mistretta (1990) found molecular evidence of hybridization between the endangered A. dendroideus var.
traskiae (Eastw. ex Abrams) Brouillet and A. argophyllus var. argenteus (Dunkle) Brouillet on San Clemente Island; however, our more detailed genetic
work suggests that hybridization among taxa is
limited to populations heavily impacted by human
activities (M. E. McGlaughlin, unpubl. data). No specific studies have been conducted examining dispersal
or pollination in Acmispon, but plants have been
documented being visited by generalist bees on Santa
Cruz (Thorp, Wenner & Barthell, 1994).
Acmispon argophyllus and A. dendroideus offer
many advantages in investigating the equilibrium
theory of biogeography as it relates to genetic diversity. First, the island varieties are insular endemics,
which implies that rates of dispersal from the mainland (or gene flow through pollen movement) are low
enough to permit insular evolution. Second, the
species appear to form a monophyletic group with
known mainland taxa (i.e. subgenus Syrmatium;
Allan & Porter, 2000), which allows sampling of
appropriate mainland relatives to examine relative
levels of genetic diversity. Third, both species are
found on several islands, both in the northern and
southern groups; this allows us to sample islands that
vary in size and distance to the mainland, in order to
untangle the impact of island characteristics on
genetic diversity. In the present study, we use the
unique features of the Channel Island endemic Acm-
ispon taxa to investigate: (1) the relationship between
island characteristics (area, distance to the mainland,
distance to nearest island, plant diversity) and
genetic diversity; (2) whether island populations have
reduced levels of genetic diversity relative to populations of mainland taxa with similar life history traits.
To achieve these goals, we have utilized a detailed
sampling of varieties and islands and have collected
genetic data from nuclear microsatellites, a low-copy
nuclear gene region (alcohol dehydrogenase), and
three plastid loci.
MATERIAL AND METHODS
STUDY SYSTEM
Relative to other well-studied island systems, the
Channel Islands are unique because of their close
proximity to the mainland (Table 1), which may
increase the frequency of successful mainland to
island dispersal. The Channel Islands are composed
of four northern islands (San Miguel, Santa Rosa,
Santa Cruz and Anacapa) and four southern islands
(San Nicolas, Santa Barbara, Santa Catalina and San
Clemente; Fig. 1). The northern islands are close to
the mainland and to each other, forming a single
large island, Santa Rosae, during recent glacial
advances (Vedder & Howell, 1980). Although never
connected to the mainland, Santa Rosae is estimated
to have been separated from it by as little as 6 km
during the last glacial maxima (Junger & Johnson,
1980). The southern islands are considerably further
from each other and the mainland and have always
been separated from the mainland by broad deepwater channels. Island age has been difficult to document in this system. The oldest volcanic rocks on both
the northern and southern islands formed approximately 19 Mya (Gordon, 2009), but, because of highly
variable uplift rates, the age of specific islands is
unclear. Further complicating our understanding of
Table 1. California Channel Island characteristics (plant data from Moody, 2009)
Distance (km)
Island
Area (km2)
Mainland
Nearest island
Native species
Exotic species
Total plant species
San Miguel
Santa Rosa
Santa Cruz
Anacapa
San Nicolas
Santa Barbara
Santa Catalina
San Clemente
37
217
249
2.9
58
2.6
194
145
42
44
30
20
98
61
32
79
6
6
8
8
45
39
34
34
198
387
480
190
139
88
421
272
69
98
170
75
131
44
185
110
267
485
650
265
270
132
606
382
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
island age is that the islands with limited topography
(San Nicolas, Santa Barbara and San Miguel) were
probably submerged during periods of maximum
Pleistocene sea levels (Vedder & Howell, 1980).
Despite their proximity to the mainland, the
Channel Islands harbour a unique flora (Philbrick &
Haller, 1977; Wallace, 1985), with 9–17% of native
plant species represented by island endemics (Moody,
2009). Philbrick & Haller (1977) described 12 plant
communities on the Channel Islands. All eight islands
contain Valley and Foothill Grassland, and seven of
the eight islands contain Coastal Bluff and Coastal
Sage Scrub, the most abundant island plant community. The three largest islands (Santa Rosa, Santa
Cruz and Santa Catalina) are topographically more
diverse and also contain woodlands, including Southern Coastal Oak Woodland, Island Woodland (also
found on San Clemente), and Bishop Pine Forests
(Santa Rosa and Santa Cruz) and Island Chaparral.
The southern islands, which are drier than the northern islands, also contain Maritime Cactus Scrub
(San Clemente and Santa Catalina). Annual rainfall
ranges from as little as 150 mm on San Clemente to
310 mm on Santa Catalina and 500 mm on Santa
Cruz (Junak et al., 1995; Schoenherr et al., 2010).
STUDY
SPECIES
Acmispon argophyllus consists of five varieties, two of
which occur on the mainland, A. argophyllus var.
argophyllus and A. argophyllus var. fremontii
(A.Gray) Brouillet, and three of which are endemic to
the Channel Islands, A. argophyllus var. adsurgens
(Dunkle) Brouillet, A. argophyllus var. argenteus and
A. argophyllus var. niveus (Greene) Brouillet. The
Channel Islands representatives are found on all four
southern and one northern island (Fig. 1). Acmispon
dendroideus consists of three varieties endemic to the
Channel Islands, A. dendroideus (Greene) Brouillet
var. veatchii (Greene) Brouillet, A. dendroideus var.
dendroideus and A. dendroideus var. traskiae, found
on all four northern and two southern islands (Fig. 1).
Acmispon glaber (Vogel) Brouillet has been identified
as the closest mainland relative of A. dendroideus
based on morphology (Isley, 1981), with the two
species formerly sharing a circumscription.
SAMPLING
One to three populations were sampled for each taxon
on each island (Fig. 1; Table S1). A least 30 individuals were sampled from each population, with 30 and
ten to 12 individuals being sampled for microsatellite
and DNA sequencing analyses, respectively. For
A. dendroideus we sampled 14 populations: A. dendroideus var. veatchii San Miguel (2); A. dendroideus
293
var. dendroideus Santa Rosa (2), Santa Cruz (3),
Santa Catalina (3), Anacapa (1); and A. dendroideus
var. traskiae San Clemente (3). For A. argophyllus we
sampled 15 California Channel Island populations:
A. argophyllus var. adsurgens San Clemente (3);
A. argophyllus var. argenteus San Clemente (3),
Santa Catalina (3), San Nicolas (2) Santa Barbara (1);
and A. argophyllus var. niveus Santa Cruz (3). Three
outgroup taxa were sampled: A. argophyllus var.
argophyllus (2); A. argophyllus var. fremontii (1); and
A. glaber var. glaber (2). The microsatellite data set
includes a more limited sampling for the following
taxa and islands: A. dendroideus var. dendroideus
Santa Rosa (1), Santa Cruz (2), Santa Catalina (1),
A. argophyllus var. adsurgens San Clemente (1); and
A. argophyllus var. argenteus San Clemente (2).
Genomic DNA was extracted from frozen leaf tissue
using a modified cetyl trimethylammonium bromide
(CTAB) protocol (Friar, 2005) or the Qiagen DNeasy
Plant Mini Kit (Valencia, CA, USA).
NUCLEAR
MICROSATELLITES
Fifteen microsatellite primer pairs developed for
Acmispon were used to gather data for all individuals
(McGlaughlin et al., 2011). Amplification was carried
out in a 12-μL reaction on an MJ Research PTC200, Eppendorf Mastercycler EP or Bio-Rad S1000
thermal
cycler,
following
the
protocols
in
McGlaughlin et al. (2011). Amplification products
were diluted with water and combined into multiplexes containing two to five loci each, depending on
the population. Each multiplex was electrophoresed
with the LIZ-500 size standard on an Avant-3100
Genetic Analyzer (Applied Biosystems, Foster City,
CA, USA), following the manufacturer’s instructions.
Fragments were sized with GeneMapper version 3.7
(Applied Biosystems).
ALCOHOL
DEHYDROGENASE SEQUENCING
Degenerate primers were developed for the gene
region alcohol dehydrogenase (ADH) using aligned
mRNA sequences and the complete genome of Lotus
japonicus (Regel) K.Larsen (available from GenBank).
Amplifications were conducted in a 25-μL volume,
which contained 1 × GoTaq Flexi Buffer (Promega,
Madison, WI, USA), 2 mM magnesium chloride
(MgCl2), 1 μL deoxynucleotide triphosphates (dNTPs)
(at 2.5 mM; Promega), 0.2 μM of each primer,
1 × bovine serum albumin (New England Biolabs,
Ipswich, MA, USA), 1 unit GoTaq DNA Polymerase
(Promega) and 1 μL DNA (10–20 ng). The thermal
cycling profile was one cycle of 94 °C for 2 min, 30
cycles of 94 °C for 1 min, 57.4 °C for 1 min, 72 °C for
4 min, one cycle of 72 °C for 1 min. PCR products
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
294
M. E. MCGLAUGHLIN ET AL.
were cloned using pGEM-T Easy cloning kits
(Promega), followed by re-suspension of individual
colonies in TE buffer for direct sequencing. After
initial sequencing with degenerate primers, a single
copy of ADH (ADH-A) was selected for further analyses. The forward primer, ADH-A_E1_F (GCAGAGGT
CAAACATTTTCATT), is positioned at the 3′ end of
L. japonicus ADH exon 1. The reverse primer, ADHA_E4_R1 (TGGACAACATGATACCAACATT), is positioned at the 5′ end of L. japonicus ADH exon 4. Two
internal primers, ADH-A_IF (GTGGCAAAGGGAG
GTGTAGA) and ADH-A_IR (GAATAATCGAGGGTGT
GTTGC), were used to obtain complete double
stranded data of all sequenced clones. Cleaned products were sequenced in the forward and reverse directions using Big Dye Terminator V.3.1 chemistry
(Applied Biosystems) in 10-μL reactions. Sequenced
samples were cleaned using Sephadex G-50 fine (GE
Healthcare, Piscataway, NJ, USA) in flow-through
columns and submitted to the Arizona State University DNA Laboratory (Tempe, AZ, USA) for capillary
electrophoresis. A consensus sequence of each region
for each sample was generated from the forward and
reverse sequences using Sequencher v. 4.1 (GeneCodes, Ann Arbor, MI, USA). For each sampled individual, three to five clones were sequenced to screen
for paralogues. The single most common sequence
was used for all analyses. In A. dendroideus from the
northern islands, a divergent ADH-B copy was initially found in 34 out of 80 sampled individuals.
Individuals containing the divergent copy underwent
additional cloning until the ADH-A copy was
retrieved. Nineteen individuals were excluded from
analyses because the ADH-A copy was not found.
Sequences were aligned for each region by eye using
Se-AL (Rambaut, 1996). Sequences are deposited in
GenBank under accession numbers KF055473 to
KF055825.
PLASTID DNA
SEQUENCING
Three non-coding plastid loci, portions of the rpL16
and ndhA introns and the psbD-trnT intergenic
spacer, were sequenced for all samples. Primer
sequences were developed to target Acmispon. The
primers used were rpl16-321F (5′TTGTTTTGGTAT
AAGATTCG3′), rpl16-815R (5′TTCTAATATGTAAGG
GTCTGTGGGTA3′), ndhA-531F (5′CACAAAGGATTC
GTAATGC3′), ndhA-1226R (5′TTTCACCTCATACGG
CTC CT3′), psbD-trnT-586F (5′GAGACCGACCCAT
ACGAAAT3′) and psbD-trnT-1228R (5′TCTCGTATA
CTGCCCCTTCG3′). Amplification reactions were conducted in a 25-μL volume, which contained 1 × GoTaq
Flexi Buffer (Promega), 2 mM MgCl2, 160 μM of each
dNTP (Promega), 0.2 μM of each primer, 1 × bovine
serum albumin (New England Biolabs), 0.5 units
GoTaq DNA Polymerase (Promega) and 1 μL DNA
(10–20 ng). The thermal cycling profile was one cycle
of 80 °C for 5 min, 30 cycles of 95 °C for 1 min,
50–65 °C for 1 min (+ 0.3 °C s−1 from 50 °C to 65 °C),
65 °C for 5 min, one cycle of 65 °C for 5 min. Amplification products were verified on 1.5% agarose gels,
followed by cleaning the remaining product with
6.25 units of Exonuclease I (New England Biolabs),
1.25 units of Antarctic Phosphatase (New England
Biolabs) and 0.1 × Antarctic Phosphatase Buffer in a
thermal cycler (37 °C for 15 min and 80 °C for 15 min).
Sequencing procedures followed those described for
the ADH region. Sequences are deposited in GenBank
under accession numbers KF042892–KF044258. For
analysis, the three sequences for each individual were
concatenated into a single cpDNA haplotype.
GENETIC
DIVERSITY ANALYSES
Microsatellites were analysed using GenAlEx
version 6.5 (Peakall & Smouse, 2012) to determine
number of alleles per locus (Na), effective number of
alleles per locus (Ne), observed (HO) and expected (HE)
heterozygosity and inbreeding coefficients (FIS).
Deviations from the Hardy–Weinberg equilibrium
were assessed using Genepop on The Web version 4.2
(Raymond & Rousset, 1995). DNA sequences were
analysed using DnaSP version 5.10.1 (Rozas et al.,
2003) to determine nucleotide diversity (π), number of
segregating sites (S), number of haplotypes (H), haplotype diversity (Hd) and Wattersons population
mutation parameter averaged by site (θsite). Twotailed t-tests to determine significant differences
between diversity estimates for island and mainland
populations were performed using SigmaPlot 12.3
(SystatSoftware, San Jose, CA, USA). For all t-tests,
normality was assessed using the Shapiro–Wilk
statistic and the equal variance test with P < 0.05.
When data were not normally distributed, the nonparametric Mann–Whitney U-test was conducted.
Island taxa were compared with close mainland
relatives with similar life history characteristics,
island A. argophyllus with mainland A. argophyllus
and A. dendroideus to A. glaber. All diversity statistics were calculated individually for populations and
then averaged by island for comparisons; mainland
populations were treated singly.
REGRESSION
ANALYSES
The relationship between genetic diversity and island
area, distance to the mainland, distance to the
nearest island and number of plant species on an
island [used to assess SGDC following Vellend,
(2003)] was calculated with multiple stepwise regression (forward stepwise procedure) using SPSS Statis-
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
tics version 20 (IBM, Armonk, NY, USA). Island area,
distance to the mainland and number of plants
species were obtained from Moody (2009). Distance to
the nearest islands was calculated using Google
Earth 7.1.1.1888 (Google Inc., Mountain View, CA,
USA), drawing a straight line between solid land on
all adjacent islands. Multiple measurements were
conducted for each island pair and distances were
rounded to the nearest kilometre. Multiple stepwise
regression tests for a relationship between a dependent variable (measures of genetic diversity) and multiple independent variables (island characteristics) to
determine which independent variables individually
or in combination have the greatest influence on
the dependent variable. Multiple stepwise regression
analyses were conducted for the two species sampled
from multiple islands individually and with all island
samples combined. Microsatellite inbreeding coefficients (FIS), A. argophyllus ADH haplotype diversity
(Hd) and A. dendroideus number of plastid haplotypes
(H) were excluded from regression analyses because
values were not normally distributed.
RESULTS
Twenty-three and 29 island populations of Acmispon
were sampled for microsatellites and DNA sequence
data sets, respectively. Five mainland populations
295
were sampled for all data sets. The microsatellite
data set included 983 individuals, with an average
sampling of 30.7 individuals per population. For the
microsatellite data set, the observed number of alleles
(Na), expected number of alleles (Ne), observed heterozygosity (HO), expected heterozygosity (HE) and
inbreeding coefficient (FIS) are shown for all populations in Table 2. Over all populations, 50% of sampled
loci showed deviations from Hardy–Weinberg equilibrium (data not shown). No single locus deviated from
Hardy–Weinberg equilibrium for all populations, suggesting that deviations are caused by population level
processes. At the population level, all sampled populations deviated from Hardy–Weinberg equilibrium,
except for A. argophyllus var. argenteus on Santa
Barbara, which was monomorphic for 14 of the 15
sampled loci (data not shown). Populations of A. dendroideus exhibited higher genetic diversity than
A. argophyllus for all microsatellite diversity measures (Table 2). Additionally, A. dendroideus was significantly less diverse than its close mainland relative
A. glaber for Na, Ne and HE. There were no significant
differences in levels of microsatellite diversity
between mainland and island populations of A. argophyllus (Table 2). Acmispon argophyllus and A. dendroideus FIS values were not normally distributed, but
a subsequent Mann–Whitney U-test did not find significant differences for either of the mainland–island
Table 2. Microsatellite DNA diversity statistics for Acmispon from the California Channel Islands and adjacent mainland
Species
Variety
Island
N
Number of
populations
A. dendroideus – island
veatchii
dendroideus
dendroideus
dendroideus
dendroideus
traskiae
Mean
glaber
niveus
argenteus
argenteus
argenteus
argenteus
adsurgens
Mean
argophyllus
fremontii
Mean
San Miguel
Santa Rosa
Santa Cruz
Anacapa
Santa Catalina
San Clemente
29.93
27.27
30.00
22.07
24.33
30.09
2
1
2
1
2
3
Santa Cruz
San Nicolas
Santa Barbara
Santa Catalina
San Clemente
San Clemente
30.80
29.29
27.00
32.00
27.36
24.90
39.93
2
3
2
1
3
2
1
26.90
25.47
2
1
A. glaber – mainland
A. argophyllus – island
A. argophyllus –
mainland
Na
Ne
HO
HE
FIS
4.13
4.13
6.17
3.00
4.00
3.64
4.18
6.00
2.84
3.50
1.27
4.82
4.53
2.67
3.27
3.23
3.80
3.42
2.23
2.34
2.95
1.81
2.35
1.93
2.27*
3.18*
1.50
1.87
1.02
2.72
2.66
1.69
1.91
1.72
2.28
1.91
0.33
0.30
0.40
0.07
0.33
0.22
0.28
0.46
0.07
0.18
0.01
0.35
0.29
0.18
0.18
0.18
0.39
0.25
0.42
0.45
0.53
0.36
0.42
0.34
0.42*
0.59*
0.25
0.33
0.02
0.49
0.51
0.33
0.32
0.31
0.45
0.36
0.35
0.26
0.73
0.23
0.31
0.20
0.28
0.18
0.48
0.42
0.25
0.42
0.21
0.66
0.40
0.38
0.22
0.33
Mainland–island species pairs were compared for significant differences based on two-tailed t-tests; *P < 0.05.
Na, number of observed alleles; Ne, effective number of alleles; HO, observed heterozygosity; HE, expected heterozygosity;
FIS, inbreeding coefficient.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
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M. E. MCGLAUGHLIN ET AL.
Table 3. DNA sequence diversity for the nuclear alcohol dehydrogenase (ADH) region for Acmispon from the California
Channel Islands and adjacent mainland
Species
Variety
Island
Number of
populations
N
π
S
H
Hd
θsite
A. dendroideus –
island
veatchii
dendroideus
dendroideus
dendroideus
dendroideus
traskiae
Mean
glaber
niveus
argenteus
argenteus
argenteus
argenteus
adsurgens
Mean
argophyllus
fremontii
Mean
San Miguel
Santa Rosa
Santa Cruz
Anacapa
Santa Catalina
San Clemente
2
2
3
1
3
3
7.50
6.00
8.67
7.00
9.00
10.33
Santa Cruz
San Nicolas
Santa Barbara
Santa Catalina
San Clemente
San Clemente
2
3
2
1
3
3
3
10
10.00
9.00
9.00
9.67
10.00
10.33
2
1
10
10
0.003
0.006
0.006
0.002
0.006
0.005
0.004*
0.008*
0.002
0.004
0.006
0.005
0.004
0.003
0.004
0.003
0.005
0.004
8.50
14.00
18.00
7.00
14.67
19.67
13.64*
27.50*
9.00
13.00
22.00
19.67
14.33
12.00
15.00
11.00
13.00
11.67
6.00
5.50
8.00
5.00
7.33
10.00
6.97
9.50
6.67
7.00
9.00
9.33
9.67
7.67
8.22
7.00
6.00
6.66
0.925
0.967
0.979
0.857
0.948
0.993
0.945
0.991
0.889
0.925
1.000
0.993
0.993
0.893
0.949
0.867
0.844
0.859
0.004
0.007
0.008
0.003
0.006
0.007
0.006‡
0.011‡
0.003
0.004
0.006
0.007
0.006
0.005
0.005
0.004
0.005
0.004
A. glaber – mainland
A. argophyllus –
island
A. argophyllus –
mainland
Mainland–island species pairs were compared for significant differences based on two-tailed t-tests; *P < 0.05, ‡P < 0.001.
π, nucleotide diversity; S, number of segregating sites; H, number of haplotypes; Hd, haplotype diversity; θsite, Wattersons
population mutation parameter averaged by site.
comparisons (A. argophyllus FIS U = 5.00, P = 0.38;
A. dendroideus FIS U = 2.00, P = 0.286).
For the ADH and plastid data sets, number of
plastid haplotypes (N), nucleotide diversity (π),
number of segregating sites (S), number of haplotypes
(H), haplotype diversity (Hd) and theta per site (θsite)
are shown in Tables 3 and 4, respectively. The ADH
data set included 324 samples and the aligned
sequence length was 957 nucleotides. The plastid
data set included 420 samples and the aligned
sequence length was 1629 nucleotides (ndhA intron –
588 bp; psbD-trnT IGS – 587 bp; rpl16 intron –
454 bp). Acmispon dendroideus populations had
significantly smaller values of π, S and θsite than
A. glaber for the ADH data (Table 3) and S and θsite for
the plastid data (Table 4). No significant differences
in ADH or plastid diversity were observed when comparing mainland and island populations of A. argophyllus (Tables 3 and 4). Measures of A. argophyllus
ADH haplotype diversity and A. dendroideus plastid
number of haplotypes were not normally distributed,
but subsequent Mann–Whitney U-tests did not find
significant differences in these values for any of the
comparisons (A. argophyllus ADH haplotype diversity
U = 3.00, P = 0.167; A. dendroideus plastid number of
haplotypes U = 6.00, P = 1.00).
Stepwise regression models between microsatellite
genetic diversity and the predictor variables were not
significant (P < 0.05) (Table 5), but significant regression models were found for the ADH (Table 6; Fig. 2)
and plastid DNA data sets (Table 7; Fig. 3). Significant (P < 0.05) multiple stepwise regression models
were found for ADH diversity for the response variables A. dendroideus π, A. dendroideus θsite, all island
populations number of segregating sites and all
island populations number of haplotypes (Table 6;
Fig. 2). All significant ADH diversity predictor variables were positively related based on the standard
partial regression (β) coefficients (Table 6). Acmispon
dendroideus π was predicted by island area (R =
0.989, P < 0.001), A. dendroideus θsite was predicted by
island area (R = 0.963, P = 0.002), all island populations number of segregating sites was predicted by
distance to nearest island (R = 0.597, P = 0.040) and
all island populations number of haplotypes was
predicted by distance to nearest island (R = 0.706,
P = 0.010) (Table 6). Significant (P < 0.05) multiple
stepwise regression models were found for plastid
diversity for all island populations response variables
π, number of segregating sites, haplotype diversity
and θsite (Table 7; Fig. 3). Plant diversity was the
only significant predictor variable with a positive
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
297
Table 4. DNA sequence diversity for the combined plastid data set for Acmispon from the California Channel Islands and
adjacent mainland
Species
Variety
Island
Number of
populations
N
π
S
H
Hd
θsite
A. dendroideus –
island
veatchii
dendroideus
dendroideus
dendroideus
dendroideus
traskiae
Mean
glaber
niveus
argenteus
argenteus
argenteus
argenteus
adsurgens
Mean
argophyllus
fremontii
Mean
San Miguel
Santa Rosa
Santa Cruz
Anacapa
Santa Catalina
San Clemente
2
2
3
1
3
3
12.0
12.0
12.0
12.0
11.7
12.0
Santa Cruz
San Nicolas
Santa Barbara
Santa Catalina
San Clemente
San Clemente
2
3
2
1
3
3
3
12.5
12.0
12.0
12.0
12.0
12.0
12.0
2
1
12.0
12.0
0.001
0.000
0.003
0.000
0.002
0.001
0.001
0.003
0.002
0.002
0.000
0.002
0.001
0.000
0.001
0.000
0.000
0.001
7.50
2.00
8.00
1.00
8.00
3.00
4.92*
12.00*
9.33
7.00
0.00
9.67
8.67
1.67
6.06
1.00
1.00
1.00
4.00
1.50
3.33
2.00
3.33
2.00
2.69
3.00
4.67
3.50
1.00
4.33
4.00
2.00
3.25
1.50
2.00
1.67
0.523
0.152
0.606
0.167
0.434
0.515
0.399
0.561
0.571
0.463
0.000
0.722
0.571
0.162
0.415
0.152
0.409
0.237
0.002
0.000
0.002
0.000
0.002
0.001
0.001*
0.003*
0.002
0.001
0.000
0.002
0.002
0.000
0.001
0.000
0.000
0.001
A. glaber – mainland
A. argophyllus –
island
A. argophyllus –
mainland
Mainland–island species pairs were compared for significant differences based on two-tailed t-tests; *P < 0.05.
π, nucleotide diversity; S, number of segregating sites; H, number of haplotypes; Hd, haplotype diversity; θsite, Wattersons
population mutation parameter averaged by site.
Table 5. Multiple stepwise regression analyses (forward procedure) of island area, distance to mainland, distance to
nearest island and plant diversity (number of plant species) on measures of microsatellite genetic diversity
ANOVA
Diversity
measure
Variable
A. dendroideus
Ne (R = 0.802)
HO
HE
Plant diversity
0.002
2.689
No significant relationship
No significant relationship
A. argophyllus
Ne
HO
HE
No significant relationship
No significant relationship
No significant relationship
All Island
Populations
Ne (R = 0.567)
Plant diversity
0.567
HO (R = 0.524)
Plant diversity
HE (R = 0.536)
Plant diversity
Taxon
β
t
d.f.
Mean
square
P
Source
F ratio
0.055
Regression
Residual
1
4
0.518
0.072
7.232
2.175
0.055
1.947
0.080
0.536
2.009
0.072
1
10
1
10
1
10
1.099
0.232
0.049
0.013
0.062
0.015
4.732
0.524
Regression
Residual
Regression
Residual
Regression
Residual
3.789
4.035
Only models with P < 0.10 and the significant predictor variables are shown.
Na, number of observed alleles; Ne, effective number of alleles; HO, observed heterozygosity; HE, expected heterozygosity;
R, multiple correlation coefficient; β, standardized partial regression coefficient; t, t-statistic (two-tailed test of whether
the partial regression coefficient differs from zero); d.f., degrees of freedom; P, significance probability.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
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M. E. MCGLAUGHLIN ET AL.
Table 6. Multiple stepwise regression analyses (forward procedure) of island area, distance to mainland, distance to
nearest island and plant diversity (number of plant species) on measures of ADH DNA sequence diversity
ANOVA
Diversity
measure
Taxon
Variable
A. dendroideus π (R = 0.989)
S
H
Hd
θsite (R = 0.963)
β
t
P
Source
Island area
0.989 13.425 < 0.001 Regression
No significant relationship
Residual
No significant relationship
No significant relationship
Island area
0.963 7.164
0.002 Regression
Residual
A. argophyllus
π (R = 0.758)
S
H
θsite
Distance to mainland
0.758
No significant relationship
No significant relationship
No significant relationship
All island
populations
π
θsite
S (R = 0.597)
Mean
d.f. square
F ratio
1
4
< 0.001 180.238
< 0.001
1
4
< 0.001
< 0.001
51.321
2.321
0.081 Regression
Residual
1
4
< 0.001
< 0.001
5.388
No significant relationship
No significant relationship
Distance to nearest island 0.597
2.356
Distance to nearest island 0.706
3.153
90.250
16.255
15.054
1.514
5.552
H (R = 0.706)
0.040 Regression 1
Residual
10
0.010 Regression 1
Residual
10
Hd
θsite
No significant relationship
No significant relationship
9.944
Only models with P < 0.10 and the significant predictor variables are shown.
π, nucleotide diversity; S, number of segregating sites; H, number of haplotypes; Hd, haplotype diversity; θsite, Wattersons
population mutation parameter averaged by site; R, multiple correlation coefficient; β, standardized partial regression
coefficient; t, t-statistic (two-tailed test of whether the partial regression coefficient differs from zero); d.f., degrees of
freedom; P, significance probability.
A A. dendroideus ADH
Island area (km2)
Island area vs. π
B All island Acmispon ADH
Distance to nearest island (km)
Distance to nearest island vs. H
Distance to nearest island vs. S
Figure 2. Linear regression plots showing the relationship between significant predictor variables (P < 0.05) and ADH
genetic diversity. A, Acmispon dendroideus π (R2 = 0.978, P < 0.001) and θsite (R2 = 0.928, P = 0.002) vs. Island Area. B, all
island Acmispon H (R2 = 0.499, P = 0.010) and S (R2 = 0.357, P = 0.040) vs. distance to nearest island. Detailed multiple
stepwise regression (forward selection) results are provided in Table 6.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
299
Table 7. Multiple stepwise regression analyses (forward procedure) of island area, distance to mainland, distance to
nearest island and plant diversity (number of plant species) on measures of plastid DNA sequence diversity
ANOVA
Diversity
measure
Variable
A. dendroideus
π
S
Hd
θsite
No
No
No
No
A. argophyllus
π (R = 0.739)
S
H
Hd
θsite
Distance to mainland −0.739
No significant relationship
No significant relationship
No significant relationship
No significant relationship
All Island
Populations
π (R = 0.706)
Plant diversity
S (R = 0.623)
Taxon
β
d.f.
Mean
square
Regression
Residual
1
4
< 0.001
< 0.001
4.822
Regression
Residual
Regression
Residual
Regression
Residual
Regression
Residual
Regression
Residual
1
10
1
10
1
10
1
10
1
10
< 0.001
< 0.001
56.019
8.851
4.386
1.188
0.198
0.037
< 0.001
< 0.001
9.941
t
P
Source
−2.196
0.093
0.706
3.153
0.010
Plant diversity
0.623
2.516
0.031
H (R = 0.519)
Plant diversity
0.519
1.921
0.084
Hd (R = 0.589)
Plant diversity
0.589
2.303
0.044
θsite (R = 0.600)
Plant diversity
0.600
2.372
0.039
significant
significant
significant
significant
F ratio
relationship
relationship
relationship
relationship
6.329
3.691
5.305
5.625
Only models with P < 0.10 and the significant predictor variables are shown.
π, nucleotide diversity; S, number of segregating sites; H, number of haplotypes; Hd, haplotype diversity; θsite, Wattersons
population mutation parameter averaged by site; R, multiple correlation coefficient; β, standardized partial regression
coefficient; t, t-statistic (two-tailed test of whether the partial regression coefficient differs from zero); d.f. = degrees of
freedom; P = significance probability.
relationship based on the standard partial regression
(β) coefficients with all response variables: π
(R = 0.706, P = 0.010), number of segregating sites
(R = 0.623, P = 0.031), haplotype diversity (R = 0.589,
P = 0.044) and θsite (R = 0.600, P = 0.039) (Table 7).
DISCUSSION
Our results are useful for understanding the equilibrium theory of biogeography of MacArthur and
Wilson applied to levels of genetic diversity on oceanic
islands that are close to a continental source. We have
demonstrated that the relationship between island
area and genetic diversity holds for the ADH genetic
region in one species, A. dendroideus; however, this
pattern is not maintained across other species and
markers (Tables 5–7; Fig. 2). Additionally, we found
that there is no support for island isolation, at least
as measured by distance to mainland, being a significant predictor of levels of genetic diversity. When
considering all island populations, proximity to neighbouring islands and plant species diversity were posi-
tive predictors of genetic diversity for ADH (Table 6;
Fig. 2) and plastid (Table 7; Fig. 3) sequence data,
respectively. These results indicate that the equilibrium theory of biogeography is not supported by
measures of genetic diversity in Acmispon on the
California Channel Islands.
The most well-established component of the equilibrium theory of biogeography is the island area–
species diversity relationship (Losos et al., 2009). This
relationship is broadly supported for plant species
diversity on the California Channel Islands (Moody,
2000). Population genetic theory suggests that the
larger number and size of populations expected on
larger islands should result in higher cumulative
levels of diversity on an island and therefore levels
of genetic diversity on islands should correlate with
island area. We are aware of only one previous study
in plants (Yamada & Maki, 2012) that has directly
addressed this relationship; this study did not find
a significant correlation between island area and
genetic diversity. We found that island area was only
a predictor for two measures of ADH sequence diver-
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
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M. E. MCGLAUGHLIN ET AL.
B All island Acmispon plastid
S
A All island Acmispon plastid
Plant diversity
Plant diversity vs. π
Plant diversity vs. θsite
Plant diversity
Plant diversity vs. S
Hd
C All island Acmispon plastid
Plant diversity
Plant diversity vs. Hd
Figure 3. Linear regression plots showing the relationship between significant predictor variables (P < 0.05) and plastid
genetic diversity. A, all island Acmispon π (R2 = 0.499, P = 0.010) and θsite (R2 = 0.360, P = 0.039) vs. plant diversity. B, all
island Acmispon S (R2 = 0.388, P = 0.031) vs. plant diversity. C, all island Acmispon Hd (R2 = 0.347, P = 0.044) vs. plant
diversity. Detailed multiple stepwise regression (forward selection) results are provided in Table 7.
sity in A. dendroideus (Table 6; Fig. 2), with no significant effect on other genetic regions or the other
sampled species. It is important to note that many of
the measures of genetic diversity were not statistically independent because there were multiple measures of diversity derived from single genetic data sets
and our two focal species were analysed individually
and as a group. However, based on our results, the
finding that a correlation between levels of genetic
diversity and island area is not common appears to be
a sound conclusion in this system. One possible explanation for this result is that, although a larger island
is capable of sustaining more populations of a species,
populations are still discrete entities impacted by
local demographic factors (i.e. effective population
size) that will be more significant determinants of
levels of genetic diversity than the total number of
populations (Chung et al., 2004; Su et al., 2010;
García-Verdugo et al., 2013). An additional factor
impacting levels of diversity is population age, with
older populations most likely containing more diversity attributable to mutation than more recently
founded populations.
A negative relationship between island isolation
and genetic diversity has been established in two
previous studies in plants (Inoue & Kawahara, 1990;
Yamada & Maki, 2012). However, we were unable to
establish a significant relationship between diversity
and distance to the mainland among Channel Island
Acmispon. The most likely explanation for this result
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
BIOGEOGRAPHY OF CALIFORNIA CHANNEL ISLAND ACMISPON
is that island and mainland populations have had a
high rate of gene flow because of the close proximity
of the Channel Islands to the California mainland,
with distances ranging from 20 to 98 km (Table 1).
Both Yamada & Maki (2012) and Inoue & Kawahara
(1990) were studying plants from the Izu Islands off
the coast of Japan, which have a greater range in
distance to the mainland, 20–200 km. The distribution of islands relative to the mainland also differs in
the Izu Islands, with the islands forming a roughly
linear chain, whereas the coast of mainland California broadly wraps around the Channel Islands to the
north and the east (Fig. 1). Furthermore, proximity
of neighbouring islands was significantly correlated
with two measures of all island populations ADH
diversity (Table 6; Fig. 2), suggesting that the absolute degree of isolation could be more important than
distance to the mainland. This result could indicate
that colonization is occurring in a stepping-stone
fashion. Overall, it appears that the Channel Islands
are too close to the mainland and each other for
island isolation to be a major determinant of levels of
genetic diversity for multiple genetic regions.
Our results do lend support to the spatial–genetic
diversity correlation (SGDC) model proposed by
Vellend (2003). We found a consistent relationship
between plant species diversity and plastid measures
of genetic diversity when considering all island Acmispon (Table 7; Fig. 3). A correlation between island
size and plant diversity has previously been established (Moody, 2000) for the Channel Islands and the
larger islands are known to contain the most distinct
plant communities (Philbrick & Haller, 1977). As our
sampling of island taxa was designed to capture
the geographical range of each sampled species, we
effectively sampled populations in multiple plant
communities on each of the large islands (M. E.
McGlaughlin, pers. observ.). Therefore, the observed
plant diversity/genetic diversity correlation is likely to
be driven by ecological heterogeneity present on the
large islands. What is unclear is whether the genetic
heterogeneity on large islands, manifest as high
genetic diversity, is attributable to genetic drift
(Evanno et al., 2009; Sei, Lang & Berg, 2009), reduced
extinction rates in diverse communities (He et al.,
2008) or colonization/isolation patterns (Sei et al.,
2009; Papadopoulou et al., 2011; Messmer et al., 2012),
as proposed in other SGDC studies. As our plastid data
are most likely maternally inherited in Acmispon
(Gauthier, Lumaret & Bedecarrats, 1997), historical
colonization patterns and subsequent isolation among
populations may have been important determinants of
diversity. Further supporting this conclusion is the
observation that single populations do not contain
highly divergent plastid haplotypes, but a single taxon
within an island often has a high level of divergence
301
among populations (L. E. Wallace, unpubl. data), indicating that they may have been founded by multiple
independent colonization events. Future detailed
phylogeographic studies will be necessary to conclusively dissect colonization patterns. The fact that
the SGDC results were only observed when all island
samples were combined, supports the contention
by Papadopoulou et al. (2011) that multi-taxon
approaches are best suited to documenting species–
genetic diversity relationships. Furthermore, our
results parallel the findings by Papadopoulou et al.
(2011) that haplotype data are best suited for predicting SGDC biodiversity patterns in understudied biota.
We found mixed results when examining the genetic
diversity of island taxa and close mainland relatives.
Acmispon dendroideus had significantly lower levels of
genetic diversity than mainland A. glaber, for multiple
measures of microsatellite (Table 2), ADH (Table 3)
and plastid (Table 4) genetic diversity, even though
sampling of the former species was much greater than
that of the latter. This result supports the long-held
view that genetic diversity is generally lower in island
populations (Frankham, 1997; Franks, 2010) and may
be caused by population size differences between
A. glaber found on the mainland (1000 to ≥ 10 000
individuals) and A. dendroideus (100–500 individuals;
M. E. McGlaughlin, pers. observ.). In contrast, no
statistically significant differences in genetic diversity
were observed between island and mainland populations of A. argophyllus (Tables 2–4), despite island
populations exhibiting higher values for most
measures of diversity, particularly plastid haplotype
diversity. Island and mainland populations of A. argophyllus maintain similar, small population sizes (50–
200 individuals; M. E. McGlaughlin, pers. observ.), so
different demographic pressures are not expected to
play a large role in the maintenance of genetic diversity. The lack of significant differences between island–
mainland A. argophyllus genetic diversity may have
been impacted by sampling that was biased toward
island populations, reducing the power to assess differences in levels of diversity. Consequently, all island/
mainland genetic diversity conclusions should be
interpreted cautiously.
In most island systems, levels of genetic diversity
are compared with summary measures of diversity
(e.g. Hamrick & Godt, 1990; Hamrick et al., 1991) to
understand better the impacts of life history on diversity. Unfortunately, most other studies with island
plants have utilized allozyme makers (DeJoode &
Wendel, 1992; Ito et al., 1998; Francisco-Ortega et al.,
2000; Crawford et al., 2001), which have lower levels of
diversity than the microsatellite markers used in this
study, limiting comparisons. Additionally, no summary
of plant DNA sequence diversity exists from either
nuclear or plastid genomes. Based on Nybom’s (2004)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304
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M. E. MCGLAUGHLIN ET AL.
review of plant microsatellite marker diversity, Acmispon on the Channel Islands (Table 2) is less diverse
than both short-lived (HO = 0.53, HE = 0.55) and longlived (HO = 0.63, HE = 0.68) perennials, species with
mixed mating systems (HO = 0.51, HE = 0.60) or predominantly outcrossing species (HO = 0.63, HE = 0.65)
and similar in levels of diversity to endemic taxa
(HO = 0.32, HE = 0.42). When compared with available
microsatellite data for Channel Island plants,
Acmispon is more diverse than the perennial herb
Lithophragma maximum Bacig. (HO = 0.22, HE = 0.23;
Furches et al., 2009), less diverse than the perennial
shrub Galium catalinense A.Gray subsp. acrispum
Dempster (HO = 0.49, HE = 0.55; Riley et al., 2010) and
similar to the perennial shrub Crossosoma californicum Nutt. (HO = 0.33, HE = 0.38; Wallace & Helenurm,
2009). Overall, the data that exist for microsatellite
diversity in plants indicate that Channel Island Acmispon are less diverse than many continental taxa
(Nybom, 2004), but not substantially different than
other Channel Island endemic perennial taxa.
CONCLUSIONS
The research presented here demonstrates that
Channel Island Acmispon do not follow the expectations of the equilibrium theory of biogeography of
MacArthur and Wilson when examining the correlation between genetic diversity and the two most
important island characteristics (area and distance
to the mainland). Although one measure of genetic
diversity showed a positive relationship between
island area and genetic diversity, a consistent predictable pattern is not evident. We conclude that the lack
of support for the equilibrium theory of biogeography
relates to two major factors: (1) increases in island
area results in more habitat patches per island available to a species, but it does not remove the demographic pressures of individuals occurring in discrete
populations that can constrain levels of genetic diversity; (2) the Channel Islands are close enough to
each other and mainland California for dispersal to
augment genetic diversity in most populations via
repeated gene flow. Despite the lack of support for the
genetic effects predicted by the equilibrium theory of
biogeography, we did find support for SGDC based on
plastid genetic diversity. This finding indicates that
the most botanically diverse islands contain more
plastid haplotypes, and that this diversity could be
the result of more successful colonization events.
Overall, our results demonstrate the unique characteristics of the Channel Islands that allow researchers to understand patterns of evolutionary history in
an island system that is not dominated by isolation
relative to sources of colonists. This makes the
Channel Islands a model system for future research
with Acmispon and other plants to better understand
dispersal, divergence and ecological adaptation in a
near mainland island system.
ACKNOWLEDGEMENTS
This research was funded by United States National
Science Foundation awards to M.E.M. (award DEB
0842023), L.E.W. (award DEB 0842161) and K.H.
(DEB 0842332). The US Navy provided access and
logistical support for all sampling on San Clemente
and San Nicolas Islands. The Catalina Island Conservancy provided access and logistical support for
all sampling conducted on Santa Catalina Island.
Channel Islands National Park provided access and
logistical support for sampling all on San Miguel,
Santa Rosa, Anacapa and Santa Barbara Islands.
This work was performed in part at the University of
California Natural Reserve System Santa Cruz Island
Reserve on property owned and managed by The
Nature Conservancy. Mainland collecting was conducted with permission from the US Forest Service
(Los Angeles, Cleveland, and Plumas National
Forests) and California State Parks. A. Hood provided
help in collecting plastid sequence data. S. Junak
provided help in collecting specimens in the field. We
are grateful to C. García-Verdugo and two anonymous
reviewers for helpful comments on this manuscript.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Table S1. Voucher specimen numbers and GPS coordinates of taxa included in this study.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 289–304