differentiation among island populations of two Norops lizards (Reptilia: Sauria: Polychrotidae) on independently colonized islands of the Islas de Bahia (Honduras)

ORIGINALARTICLE

Genetic and morphometricdifferentiation among island populationsof two Norops lizards (Reptilia: Sauria:Polychrotidae) on independentlycolonized islands of the Islas de Bahia(Honduras)

C. F. C. Klutsch1,2*, B. Misof1, W.-R. Grosse3 and R. F. A. Moritz2

1Zoologisches Forschungsmuseum Alexander

Koenig, Adenauerallee 160, 53113 Bonn,

Germany, 2Martin-Luther-Universitat

Halle/S., Institut fur Zoologie, Hoher Weg 4,

06099 Halle/S., Germany, 3Martin-Luther-

Universitat Halle/S., Institut fur Zoologie,

Domplatz 4, 06099 Halle/S., Germany

*Correspondence: Cornelya Klutsch, KTH –

Royal Institute of Technology, Gene

Technology, Roslagstullsbacken 21, 10691

Stockholm, Sweden.

E-mail: [email protected].

ABSTRACT

Aim Anole lizards (Reptilia: Sauria: Polychrotidae) display remarkable

morphological and genetic differentiation between island populations.

Morphological differences between islands are probably due to both adaptive

(e.g. differential resource exploitation and intra- or interspecific competition) and

non-adaptive differentiation in allopatry. Anoles are well known for their extreme

diversity and rapid adaptive speciation on islands. The main aim of this study was

to use tests of morphological and genetic differentiation to investigate the

population structure and colonization history of islands of the Islas de Bahia, off

the coast of Honduras.

Location Five populations of Norops bicaorum and Norops lemurinus were

sampled, four from islands of the Islas de Bahia and one from the mainland of

Honduras.

Methods Body size and weight differentiation were measured in order to test for

significant differences between sexes and populations. In addition, individuals

were genotyped using the amplified fragment length polymorphism technique.

Bayesian model-based and assignment/exclusion methods were used to study

genetic differentiation between island and mainland populations and to test

colonization hypotheses.

Results Assignment tests suggested migration from the mainland to the Cayos

Cochinos, and from there independently to both Utila and Roatan, whereas

migration between Utila and Roatan was lacking. Migration from the mainland to

Utila was inferred, but was much less frequent. Morphologically, individuals from

Utila appeared to be significantly different in comparison with all other localities.

Significant differentiation between males of Roatan and the mainland was found

in body size, whereas no significant difference was detected between the mainland

and the Cayos Cochinos.

Main conclusions Significant genetic and morphological differentiation was

found among populations. A stepping-stone model for colonization, in

combination with an independent migration to Utila and Roatan, was

suggested by assignment tests and was compatible with the observed

morphological differentiation.

Keywords

AFLP, assignment-based methods, biogeography, Honduras, island populations,

migration, Norops, population genetics.

Journal of Biogeography (J. Biogeogr.) (2007) 34, 1124–1135

1124 www.blackwellpublishing.com/jbi ª 2007 The Authorsdoi:10.1111/j.1365-2699.2007.01691.x Journal compilation ª 2007 Blackwell Publishing Ltd

INTRODUCTION

The family Polychrotidae (Reptilia: Sauria) currently contains

over 400 described species of anoles, of which over 140 known

species inhabit Central and South America as well as several

islands in the Caribbean Sea (Williams, 1992; Powell et al.,

1996). Anole lizards display remarkable morphological and

molecular differentiation between islands (Williams, 1983;

Losos et al., 1998). Differences between islands are partly due

to non-adaptive differentiation in allopatry, but also represent

adaptive differentiation due to, for example, differential

resource exploitation as well as intra- or interspecific compe-

tition (Williams, 1983; Losos & De Queiroz, 1997a). Therefore

anole lizards appear to be ideal model organisms for studying

speciation mediated by adaptive vs. non-adaptive modes of

differentiation. Several authors have addressed problems of

speciation in anoles using a phylogenetic or taxonomic

approach (Etheridge, 1960; Williams, 1969; Guyer & Savage,

1987; Cannatella & De Queiroz, 1989; Frost & Etheridge, 1989;

Jackman et al., 1997, 1999) in order to study adaptive

speciation in this group. However, detailed studies on

differentiation processes and variation within species are rare

(Malhotra & Thorpe, 2000; Knox et al., 2001), and more

detailed information at the population level is necessary to

address speciation in this group. In an experimental approach,

Losos et al. (1997) demonstrated that founder events have led

rapidly to differentiation in morphology among island pop-

ulations. In that study, populations of Anolis sagrei, collected

from a nearby source, were introduced onto small islands and

diverged significantly within a 10–14-year period.

In the present study we focused on the genetic and

morphological differentiation of Norops populations among

the Islas de Bahia. Recently, Kohler (1996) divided the species

Norops lemurinus into two distinct species: Norops bicaorum

and N. lemurinus. Norops bicaorum has been considered as a

derived island species of N. lemurinus and is found exclusively

on Utila and Roatan, whereas N. lemurinus is distributed on

the islands of Cayos Cochinos and the mainland. In contrast,

Meyer & Wilson (1973), as well as Wilson & Cruz-Dıaz (1993),

have interpreted the morphological differences of N. bicaorum

and N. lemurinus as ‘a variety of habitat types’. In this case,

morphological differences can be interpreted as intraspecific

variation among localities, which would contradict the hypo-

thesis of two species.

In order to investigate genetic population differentiation,

our approach has encompassed the analysis of presumably

selectively neutral amplified fragment length polymorphism

(AFLP) markers. AFLP has proven to be a valuable approach to

discriminating accurately between populations of vertebrate

species (Ovilo et al., 2000). Furthermore, Ogden & Thorpe

(2002) showed that AFLP has the potential to distinguish

between species of Anolis lizards, which is essential for studies

of biodiversity in this very diverse group. However, one major

drawback is that AFLP yields dominant markers, which limits

the approach for population genetic studies (Ogden & Thorpe,

2002). Recently, improvements in statistical analysis of AFLP

data (Rannala & Mountain, 1997; Cornuet et al., 1999; Innan

et al., 1999; Zhivotovsky, 1999; Pritchard et al., 2000; Hol-

singer et al., 2002; Campbell et al., 2003; Piry et al., 2004) have

also extended the applicability of AFLP to population genetic

approaches (Bensch et al., 2002; Wang et al., 2003a,b; Takami

et al., 2004). Therefore AFLP data have become applicable to

small-scale studies of closely related species and populations, as

envisaged in our analysis.

Genetic differentiation may reflect ancient migration routes

among islands, and between islands and the mainland. Monzel

(1998) hypothesized that N. bicaorum has evolved on either

Utila or Roatan and subsequently colonized the other island.

The Cayos Cochinos islands have served as stepping-stones

and are still inhabited by N. lemurinus (hypothesis A, Fig. 1a).

Cayos Cochinos

Mainland

Roatan

Utila

Cayos Cochinos

Mainland

Roatan

Utila

Cayos Cochinos

Mainland

Roatan

Utila

(a) (b)

(c)Figure 1 Three possible migration scenar-

ios. (a) Hypothesis A (stepping-stone-model):

Norops bicaorum evolved either on Utila or

Roatan and migration between these islands

took place; (b) hypothesis B: Utila and Roatan

were colonized independently from the Cayos

Cochinos and/or the mainland; (c) hypothesis

C, in which migration took place on a con-

tinuous landscape (broken lines) before sea-

level rise (island model).

Differentiation of independent colonized islands

Journal of Biogeography 34, 1124–1135 1125ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd

An alternative hypothesis, proposed by Monzel (1998),

predicts that Utila and Roatan have been colonized independ-

ently from the Cayos Cochinos islands and/or the mainland

(hypothesis B, Fig. 1b). Again, the Cayos Cochinos have served

as stepping-stones and are currently inhabited by N. lemurinus.

Finally, Monzel (1998) suggested a third model, which assumes

that the islands were isolated during the Pliocene/Pleistocene

transition (c. 2.3 Ma) following a rise in sea level. In this case,

recent populations would be relics of a population once widely

distributed in the Pliocene (hypothesis C, Fig. 1c). If hypo-

thesis A were true, we would expect that populations on Utila

and Roatan should be genetically more similar to each other

than either is to the populations of the islands of Cayos

Cochinos. Furthermore, we would predict a unidirectional

ancient migration from the mainland to the Cayos Cochinos

islands and to one or both islands. If hypothesis B were true,

the two populations of N. bicaorum (Utila and Roatan) should

display a greater genetic dissimilarity between each other,

because of independent colonization events and subsequently

autonomous evolution. Additionally, genetic results should

reflect two independent ancient migration routes from the

Cayos Cochinos islands to both Utila and Roatan. Ancient

migration routes should also be detectable from the mainland

to both Utila and Roatan. If hypothesis C were true, we would

expect five distinct populations among our sampled localities,

without a single unidirectional ancient migration route, based

on the assumption that migration had not been strictly limited

in direction on a formerly continuous landscape (island

model). In this work, we use AFLP data in combination with

assignment tests in order to investigate potential migration

routes.

Morphological differentiation in anoles is expected to be

driven partly by adaptation to different habitats (Malhotra &

Thorpe, 1997), even at small geographical scales. A large

proportion of this adaptation is expressed in body size, colour

and shape changes. Malhotra & Thorpe (1997) found that

body size and shape variation in a Lesser Antillean anole,

Anolis oculatus, has been significantly correlated with environ-

mental variation and is under the power of natural selection.

Regarding interspecific differentiation, adaptation is equally

assumed to accentuate morphological differences between

species (Losos & De Queiroz, 1997b). For example, in the

Greater Antilles species are morphologically specialized and

occupy distinctive niches (Losos et al., 1994). Specializations

are assumed to be based on interspecific interactions (e.g.

competition). However, additional non-adaptive differenti-

ation may occur at the same time (Malhotra & Thorpe, 1997).

In both cases, body size has proven to be a suitable marker to

study morphological differentiation of anoles at the

species and population levels. Thus we used body size and

weight as a general marker for population differentiation,

without discriminating adaptive vs. non-adaptive character

differentiation. Significant differentiation in body size and

weight at the population level may indicate morphological

differentiation of populations and could support population

genetic results with regard to significant population structure.

In combination, genetic and morphological results may allow

insights into the differentiation and biogeographical history of

populations.

METHODS

Sampling

Samples were collected on four islands (Utila, Roatan, Cayo

Cochino Grande, Cayo Cochino Pequeno) of the Islas de

Bahia, a group of islands located on the Atlantic side

(Caribbean Sea) of Honduras. Additionally, one location on

the mainland, in the Pico Bonito National Park (Fig. 2), was

sampled with permission. Since islands are small and covered

with vegetation suitable for both species, every island and the

mainland locality were treated as distinct populations (see

Table 1 for information on sampling sites). Distances between

locations ranged from 11 to 70 km. In total, 175 tail tips of

N. bicaorum and N. lemurinus were collected by tail-tip

biopsies and stored in 96% ethanol until genetic analysis.

AFLP analysis

Before DNA extraction, tissue was stored in dH2O for 1 h.

Genomic DNA was extracted from tail tips using a standard

phenol–chloroform protocol (Sambrook et al., 1989). AFLP

analysis followed a modified protocol of Vos et al. (1995) and

Muller & Wolfenbarger (1999).

Restriction of genomic DNA was processed in 40 lL

containing c. 250 ng DNA, 2.5 U EcoRI, 0.5 U MseI, and

digestion buffer (33 mm Tris–acetate, 10 mm Mg-acetate,

66 mm K-acetate, 0.1 mg mL)1 BSA pH 7.0) for 2 h at room

temperature. Digestion was terminated by incubation at 65�C

for 10 min. Following restriction, a ligation mix was added

containing 1 U T4 DNA ligase, 1 lL T4 DNA ligase buffer

(330 mm Tris–acetate pH 7.8, 660 mm K-acetate, 100 mm Mg-

acetate, 5 mm (dithiothreitol) and 50 pmol lL)1 EcoRI, and

incubated overnight at 55�C. The product was diluted 1:10

Utila

RoatanGuanaja

Cayos Cochinos

La Ceiba

Belize

Guatemala

Honduras

El Salvador

Tegucigalpa

Nicaragua

Pico Bonito NP

Caribbean Sea

Figure 2 The north coast of Honduras with the five sampling

locations: Utila, Roatan, Cayos Cochinos (Cayo Cochino Grande,

Cayo Cochino Pequeno) and National Park Pico Bonito.

C. F. C. Klutsch et al.

1126 Journal of Biogeography 34, 1124–1135ª 2007 The Authors. Journal compilation ª 2007 Blackwell Publishing Ltd

with dH2O. 1 lL of this dilution was used as template in a

PCR pre-selective amplification. Pre-selective amplification

was carried out in 20 lL containing 0.3 lm EcoRI pre-selective

amplification primer, 1.5 lm MseI pre-selective amplification

Stefan Hartel and Michael Lattorff, unpublished data), 1.5 mm

MgCl2, Taq buffer, 0.4 U lL)1 Taq polymerase and 200 lm of

each dNTP. PCR was performed on a thermal cycler (9700,

Perkin Elmer, Waltham, MA, USA). After an initial denatur-

ation at 95�C for 15 min, 35 cycles were performed of 60 s at

94�C, 60 s at 56�C and 2 min at 72�C, followed by a final

elongation at 60�C for 20 min.

The pre-selective amplification product was diluted 1:10

with dH2O, and 1 lL of this dilution served as the template

for the final selective amplification. Selective amplification

was processed in 10 lL containing 1.5 mm Taq buffer,

1.5 mm MgCl2, 200 lm of each dNTP, 0.3 lm EcoRI primer

labelled with fluorescent marker, 1.5 lm MseI primer (Stefan

Hartel and Michael Lattorff, unpublished data) and

0.8 U lL)1 Taq polymerase. After an initial denaturation at

95�C for 15 min, 12 cycles were performed of 30 s at 94�C,

30 s at 65�C (temperature decreased every cycle for 0.7�C

until 56�C was reached), 2 min at 72�C, followed by 25 cycles

of 30 s at 94�C, 30 s at 56�C and 2 min at 72�C. A final

elongation of 20 min at 72�C was added. AFLP profiles were

detected by an ABI 310 sequencer according to the manu-

facturer’s instructions. To estimate fragment lengths,

GS500ROX (Applied Biosystems, Foster City, CA, USA) size

standards were included in each sample. Loading sample was

prepared in a total volume of 20 lL containing 14 lL dH2O,

3 lL PCR product, 2.5 lL loading dye (including forma-

mide) and 0.5 lL size standard. Samples were heated to 95�C

for 2 min, immediately cooled, then loaded onto an acryl-

amide gel and electrophoresed. Amplified fragments with

fluorescent signals were identified using genescan software

(Applied Biosystems). genotyper (Applied Biosystems) was

used to analyse raw data.

Population genetic analysis

Population subdivision was tested in two ways. An analysis of

molecular variance (amova) was performed to analyse the

individual pairwise genetic distance matrix. Total genetic

variation was calculated among populations within species and

within populations. Variation was summarized both as the

proportion of total variance and as U statistics. The latter is an

F-statistic analogue (Peakall et al., 1995) for AFLP data sets:

pairwise UPT was calculated among all population pairs within

species as a measurement of genetic differentiation between

populations. Statistical significance was tested by random

permutation, with the number of permutations set to 1000. In

addition, summary genetic diversity (number of polymorphic

loci, percentage of polymorphic loci, mean expected hetero-

zygosity) within and between populations was calculated. All

calculations were performed with GenAlEx (Peakall &

Smouse, 2001).

Assignment of individuals to populations

Assignment methods have been found to be especially

suitable for highly variable genetic marker systems such as

AFLPs (Cornuet et al., 1999). Two consecutive assignment

tests were executed to ensure robustness of results (Cegelski

et al., 2003).

The program structure (ver. 2.0) was used to test K, the

number of separated populations (Pritchard et al., 2000),

using a Bayesian approach based on allele frequencies. The

program calculates a posterior probability for a given K (log-

likelihood). In the present study, K ¼ 1–6 was tested at the

population level in runs for 100,000 Markov chain Monte

Carlo (MCMC) generations with a burn-in period of 100,000.

The estimated log-likelihood was used to choose the optimal

number of populations. To ensure robustness of results, each K

was tested with two independent iterations.

After calculating the most likely number of populations,

individuals were assigned to the most probable population. In

structure this is done by assessing the highest percentage of

membership using prior population information and assuming

no admixture (which is suitable for discrete populations like

those here) and correlated allele frequencies (this often

improves clustering for presumably closely related populations

like those here; Falush et al., 2003). This approach permitted

examining possible migration routes and the ancestry of

Table 1 Description of islands and the mainland site.

Island/location Size (km2) Distance between sampling sites Coordinates

Utila 41.0 Utila-Roatan: 39 km

Utila-Cayo Cochino Grande: 24 km

Utila-Cayo Cochino Pequeno 21 km

16�06¢N, 86�55¢W

Roatan 128.0 Roatan-Mainland: 70 km 16�18¢N, 86�36¢WMainland – Utila-Mainland (National Park Pico Bonito): 47 km 15�41¢N, 86�52¢WCayos Cochino Grande 1.55 Roatan-Cayos Cochino Grande: 54 km

Roatan-Cayos Cochino Pequeno: 50 km

15�54¢N, 86�54¢W

Cayos Cochino Pequeno 0.64 Cayos Cochino Grande-Mainland (National Park Pico Bonito): 25 km

Cayos Cochino Pequeno-Mainland (National Park Pico Bonito): 26.5 km

Cayos Cochino Grande-Cayos Cochino Pequeno: 11 km

15�54¢N, 86�48¢W

Data from Davidson (1979) encarta (1988–98), Wilson & Cruz-Dıaz (1993).



individuals/populations. To check whether gene flow is

ongoing or assignment is based on past migration, an

additional feature in structure was used. Probability values

for assignment were given for parent and grandparent

generations in structure when using prior population

information for individuals. The program tests whether an

individual has an immigrant ancestor in the last generations

(Pritchard et al., 2000) or represents a real-time migrant. In

GeneClass2, the Bayesian model (Baudouin & Lebrun, 2000)

in combination with the simulation algorithm of Paetkau et al.

(2004) was used to assign individuals to populations. The

threshold for assigning an individual to a population was set to

P < 0.05. This means that individuals with an assignment

value <0.05 had been assigned to the predefined population or

to any population. The latter case would indicate an origin

from an unsampled population.

Morphometric analysis

Morphological variation was studied using snout-vent length

(SVL) and weight. Body size was measured from the tip of

the snout to the anterior end of the cloaca (SVL). For weight

measurements, individuals were put into a plastic box and

placed on a standard weighing machine. All measurements

were taken from adult individuals. For Utila, additional SVL

measurements, taken in 1998–2000 in the same way, were

provided by Anne Haberberger and Kai Schreiter (unpub-

lished data), resulting in a total of 183 individuals (79 females

and 104 males). Data sets for the 3 years were tested against

each other for homogeneity with a Wilcoxon signed rank test,

and resulted in clearly non-significant differences between

data sets (females: 1998–99, 0.36; 1998–2000, 0.73; 1999–

2000, 0.07; males: 1998–99, 0.61; 1998–2000, 0.67; 1999–2000,

0.60). For analysis of weight, 144 individuals (60 females and

84 males) were taken into account. All statistical analyses

were performed with spss 12.0 for windows. Because there

was a significant sexual dimorphism regarding body size and

weight in the species studied (univariate anova: body size,

d.f. ¼ 1, P < 0.001; weight, d.f. ¼ 1, P < 0.001), all further

statistical analyses were performed separately. For both data

sets, a Kolmogorov–Smirnov test was applied to check for

normal distribution of data. A Levene test for homogeneity of

variances was applied to test equality of variances. For

females, the data set was normally distributed (size,

P < 0.354; weight, P < 0.905) but not homogenously variable

(size, P < 0.02; weight, P < 0.047). In contrast to females, the

data for males were neither normally distributed (size,

P < 0.05; weight, P < 0.05) nor equally variable (size,

P < 0.001; weight, P < 0.001). Therefore data have been

log-transformed to meet the assumptions for the following

univariate (anova) and multivariate (manova) statistics. To

study the effects of population differentiation in detail, we

applied post hoc tests to examine which groups differ

significantly from each other in one or both variables. For

both data sets, a post hoc test after Tamhane (1979) was used

because this test can also be applied when variances and

sample sizes are unequal. For multiple post hoc tests,

significant probability values were assumed at a level £0.008

(Bonferroni correction; Sokal & Rohlf, 1995).

RESULTS

In total, 145 genotypes of N. bicaorum and N. lemurinus

specimens were analysed. Only fragments with a frequency of

>0.05 were accepted, to reduce fragment patterns due to rare

artefact bands. All bands <80 bp were excluded from the

analysis as they could not be scored accurately. In total, 58

polymorphic loci were scored.

Genetic diversity and population subdivision

Descriptive parameters of genetic diversity are summarized

in Table 2. Within N. bicaorum, average heterozygosity

ranged from 0.17 to 0.20, with an average of 0.185. Within

N. lemurinus, average heterozygosity ranged from 0.24 to

0.30, with an average of 0.277. No private alleles were found

in any of the populations studied. Less common alleles

(<50% frequency) occurred in all island populations (one

rare allele in every population), but not in the mainland

population.

Table 3 summarizes the results of amova. Most variation

was distributed within populations; nevertheless a significant

among population variation was detected in N. lemurinus.

However, for populations of the Cayos Cochinos (Cayo

Cochino Grande and Cayo Cochino Pequeno), variance

among populations was not found (Table 3), thus within-

population variance accounted for 100% of the variance.

Hence for further analysis the two islands of Cayos Cochinos

were treated as a single population. Among the mainland

Table 2 Sample statistics and genetic diversity of Norops

bicaorum and Norops lemurinus calculated with GenAlEx (Peakall

& Smouse, 2001).

Locality n

Polymorphic loci

Number Percentage

Mean

expected

heterozygosity SE

N. bicaorum

Utila 36 55 91.7 0.20 0.01

Roatan 27 49 75.0 0.17 0.01

N. lemurinus

Cayo Cochino

Grande

27 53 86.0 0.24 0.02

Cayo Cochino

Pequeno

20 47 69.5 0.29 0.02

NP Pico Bonito 35 52 83.4 0.30 0.02

Polymorphic loci are defined with allele frequencies from 5% to 95%

for each population. All values are calculated based on the total

number of polymorphic loci (58). n ¼ number of individuals,

SE ¼ standard error.



population and the Cayos Cochinos, 16% of the genetic

variance was accounted for by variation among populations,

whereas the remainder (84%) represented variance among

individuals within populations. Within N. bicaorum, the

greatest proportion of variance (99%) was found within

populations; only 1% of the genetic variance was accounted for

by variation among populations. Thus no significant variance

among population has been detected within N. bicaorum.

The results of the amova were reflected by the genetic

differentiation of populations, measured as Upt. The highest

pairwise genetic differentiation was obtained between the

Cayos Cochinos and the mainland (Table 3). Between Cayo

Cochino Grande and Cayo Cochino Pequeno, as well as

between Utila and Roatan, the genetic differentiation was

found to be extremely low, with 0.001 and 0.011, respectively.

Assignment tests with STRUCTURE and GeneClass2

The most probable number of populations was found to be

K ¼ 4 (ln L ¼ )4226.0). Other values of K were less likely:

K ¼ 1 (ln L ¼ )4715.6), K ¼ 2 (ln L ¼ )4474.3), K ¼ 3

(ln L ¼ )4503.7), K ¼ 5 (ln L ¼ )4325.4), K ¼ 6 (ln L ¼)4397.4). The second iteration resulted in similar ln likeli-

hoods for each K, which indicated that a sufficient length of

burn-in time and number of generations were performed.

In structure, 111 individuals (76.6%) presented the

highest probability of fitting their assumed population assign-

ment. In GeneClass2, 112 individuals (77.2%) were assigned

to presumed populations and 33 individuals were not assigned

to presumed populations. Twenty-four individuals (17%) were

identified in both assignment tests to be immigrants from

another population. Of these 24 individuals, 17 were assigned

to the same origin populations in both tests (Table 4).

However, seven individuals (107, 119, 125, 126, 128, 129,

130) were only ambiguously assigned to a single population.

Generally, these individuals showed approximately the same

probability of being assigned to different populations. More-

over, five individuals (8, 9, 15, 73, 95) were correctly assigned

in the program structure, while GeneClass2 rejected

assigning these individuals to the presumed correct popula-

tion. Furthermore, two individuals (137, 140) were not

assigned to the presumed original population in structure,

whereas in GeneClass2 the correct population was identified,

although it should be mentioned that the same probability was

obtained for two populations in each case. In addition, seven

individuals (65–71, not shown in Table 4) showed ambiguous

results in both assignment tests. In structure these individ-

uals presented low probability (0.448–0.691) of membership

for the population where they were sampled, although

probability values were always highest in comparison with

probability values for assignment to other populations, there-

fore these individuals were still correctly assigned. In Gene-

Class2 the same individuals showed approximately the same

high probability for all four populations (0.99–1.000) in all

seven cases. In conclusion, both assignment tests proved highly

reliable, with a high overlap in identification of individuals that

did not belong to the presumed populations, and therefore

supported the robustness of the results.

Based on individuals that presented congruent assignment

in both tests (Table 4), the mainland population appeared as

the most homogenous, with the highest probability of

individuals belonging to the assumed population. Three

individuals (73, 75, 95) showed a probable assignment to the

Cayos Cochinos in GeneClass2 that could not be confirmed

in structure. Cayos Cochinos presented the highest percent-

age of individuals that had been assigned to the mainland

(c. 17%), whereas Utila showed only a very small probability of

assignment of individuals to the mainland (c. 3%). No

evidence was found for migration from the mainland to

Roatan. Both Utila and Roatan presented similar assignment

probabilities to the Cayos Cochinos (c. 11% and 15%,

respectively). Additionally, no evidence was found for a

migration between Utila and Roatan (0%). Finally, Cayos

Cochinos individuals showed no confirmed assignment to

Utila and Roatan.

Concerning the question of whether migration is still

ongoing, or individual assignment to population is based on

immigrant ancestors; the probabilities for real-time migrants

were lowest in all cases (Prt, Table 4). If individuals had been

assigned to a different population than previously assumed,

assignment probabilities were always highest at the grandpar-

ent generation (Pgp), indicating that individual assignment has

been based on immigrant ancestors at the grandparent level. As

a consequence, the results supported ancient rather than

ongoing migration.

Morphometry

Tables 5–7 summarize the results of the manova and anova

statistics. For females, manova showed highly significant

results when combining both variables for the factor species

Table 3 Results of amova to explore geographical subdivision

in populations showing the percentage of variation between

population pairs.

Locality d.f. SS MS

Percentage

variation Upt P

Norops bicaorum

Utila-Roatan

Among populations 1 11.851 11.851 1.0 0.011 NS

Within populations 61 535.991 8.787 99.0 NS

Norops lemurinus

Cayo Cochino Grande–Cayo Cochino Pequeno

Among populations 1 11.085 11.085 – 0.001 NS

Within populations 45 491.128 10.914 100.0

Mainland–Cayos Cochinos

Among populations 1 93.197 93.197 16.0 0.169 0.01

Within populations 79 836.531 10.589 84.0

d.f. ¼ degrees of freedom; SS ¼ sum of squares, MS ¼ mean squares,

Upt ¼ a measurement for population differentiation analogous to FST.



Table 4 Results of assignment tests in structure and GeneClass2.

Individual

number

Geographic

origin

Structure

population

assignment Pap Prt Pp Pgp

GeneClass2 Bayesian

assignment/exclusion

P

8 Utila Utila 0.980 Mainland 0.844

9 Utila Utila 0.899 Mainland

Cayos Cochinos

0.964

0.983

10* Utila Mainland 0.046 0.132 0.263 0.527 Mainland 1.000

11* Utila Cayos Cochinos 0.000 0.117 0.234 0.469 Cayos Cochinos 1.000

15 Utila Utila 0.986 Mainland 0.999




38* Roatan Cayos Cochinos 0.000 0.120 0.240 0.480 Cayos Cochinos 1.000




73 Mainland Mainland 0.983 Cayos Cochinos 0.534

77 Mainland Mainland 0.870 Mainland

Cayos Cochinos

0.996

1.000

95 Mainland Mainland 0.843 Cayos Cochinos 0.968

107* Cayos Cochinos Roatan 0.002 0.121 0.243 0.485 Utila 1.000

Roatan 1.000

Mainland 1.000

Cayos Cochinos 1.000

116* Cayos Cochinos Mainland 0.010 0.135 0.270 0.540 Mainland 1.000



119* Cayos Cochinos Utila 0.000 0.057 0.114 0.228 Utila 1.000

Roatan 0.046 0.091 0.183 Roatan 0.975

Mainland 0.040 0.080 0.161 Mainland 1.000





125* Cayos Cochinos Mainland 0.001 0.078 0.157 0.313 Mainland

Cayos Cochinos

1.000

1.000


Cayos Cochinos

1.000

1.000



Cayos Cochinos

1.000

1.000

129* Cayos Cochinos Utila 0.000 0.057 0.114 0.227 Utila 1.000

Roatan 0.045 0.090 0.180

Mainland 0.041 0.082 0.165 Mainland 1.000

130* Cayos Cochinos Utila

Roatan

0.000 0.056

0.070

0.111

0.141

0.223

0.281

Utila

Mainland

1.000

1.000

137 Cayos Cochinos Utila

Mainland

0.259 0.062

0.044

0.124

0.087

0.249

0.174

Mainland

Cayos Cochinos

1.000

1.000

140 Cayos Cochinos Utila 0.001 0.090 0.181 0.361 Mainland

Cayos Cochinos

1.000

1.000

Geographical assignment is shown for both methods with corresponding statistical support. *Individuals identified as ancient migrants in both tests;

Pap ¼ probability of individual being from assumed population (from sampling site); Prt ¼ probability of individual being a real-time migrant from

the population found to be the original population; Pp ¼ probability of individual having ancestry at parent level; Pgp ¼ probability of individual

having ancestry at grandparent level. For populations that have been found to be the original population in structure, only the Pap value is given

because no other values have been obtained.



as well as for populations (Table 6). For single traits, the

univariate anova obtained significant results between species

regarding size, but did not show significant results for weight

(Table 6). Significant differentiation was obtained between

populations (Table 6; Fig. 3a–d). Mean values for body size and

weight with standard error and standard deviation are given in

Table 5. After Bonferroni correction, post hoc tests revealed that

both females and males from Utila differed significantly in size

from all other populations showing largest average body sizes

(Table 7; Fig. 3a). The only exception was the Utila–mainland

relationship, which showed no significant difference. Concern-

ing size, males further showed significant differences between

Roatan and the mainland (Fig. 3c). In contrast, the picture for

weight measurements was less clear. Utila appeared to be

significantly different in weight from Roatan in both females

and males, as well as from the mainland in males (Fig. 3a–d).

For all other comparisons, weight was a weak factor (Fig. 3b,d).

In summary, an increment of body size and weight was

detected, starting from the mainland with the lowest body size

and weight, to the Cayos Cochinos and Roatan, and finally to

Utila with the largest body size and heaviest individuals. Hence

Utila was the most morphologically differentiated population

in our analysis.

DISCUSSION

Genetic and morphological population differentiation

In combination, population genetic and morphological ana-

lyses identified significant structure at the population level.

At this level the structure analysis revealed four distinct

populations, whereas the amova detected significant variance

among the mainland and the Cayos Cochinos, but a lack of

significant variance among Utila and Roatan. Clearly, the key

populations in the amova were Cayos Cochinos. They were

the genetically most distinct populations and showed the

highest genetic differentiation (Upt) from the mainland. Our

results indicated that the Cayos Cochinos were colonized by

populations from the mainland. The distinct genetic character

of the Cayos Cochinos populations may have been due to

strong drift and founder effects, because they were the smallest

islands in this study.

In contrast, morphological differentiation was less clear.

Only Utila differed from all other populations in both

variables and sexes, supporting the distinct character of Utila.

For females, no other significant difference among popula-

tions was obtained. This may have been due to the lower

sample size compared with males. One other explanation

could be that there were differential forces acting on females

and males. For example, on different islands, selection

pressures may affect males in different ways than females.

In males, body size gradually increased from the mainland to

the Cayos Cochinos, Roatan, and finally Utila, compatible

Table 5 Summary descriptive statistics for body size and weight in both species and among populations, including standard error and

standard deviation.

Mean body size

(mm) SE SD

Mean weight

(g) SE SD

$ # $ # $ # $ # $ # $ #

Norops bicaorum 60.9 58.9 0.7 0.95 3.76 5.9 5.81 5.5 0.2 0.26 1.1 1.61

Utila 63.3 60.1 1.02 1.62 3.55 7.44 6.67 6.2 1.72 0.39 0.59 1.8

Roatan 59.1 57.4 0.72 0.69 2.86 2.91 5.17 4.6 0.22 0.17 0.86 0.7

Norops lemurinus 58.4 54.3 0.8 0.45 4.59 3.02 5.54 4.5 0.22 0.09 1.26 0.61

Mainland 58.8 53.14 1.5 0.52 5.99 2.44 5.4 4.2 3.68 0.13 1.47 0.6

Cayos Cochinos 58.1 55.4 0.67 0.66 2.7 3.15 5.68 4.8 0.26 0.1 1.05 0.48

Table 6 Summary statistics for combined variables for the factor

species/populations (manova) and separate analysis of factors

(anova) for species/populations.

manova P anova P

Species Populations

Species Populations Size Weight Size Weight

Females <0.001 <0.001 <0.001 0.323 <0.001 0.005

Males <0.001 <0.001 <0.001 <0.001 <0.001 <0.001

Table 7 Results of post hoc tests for single factors (size/weight) at

the population level (only significant results shown).

Post hoc test P

Sex Location Size Weight

Females Utila–Roatan <0.001 <0.001

Females Utila–Cayos Cochinos <0.001 0.022

Females Utila–mainland <0.012 0.03

Males Utila–Roatan 0.005 0.008

Males Utila–Cayos Cochinos <0.001 0.02

Males Utila–mainland <0.001 <0.001

Males Roatan–mainland <0.001 0.01

Males Mainland–Cayos Cochinos <0.001 0.01



with the stepping-stone model of colonization. In females, an

increment in body size was found between species. In both

sexes, a key difference in the amova was that Utila and

Roatan were found to be morphologically significantly

different from one another.

The significant morphological differentiation of the popu-

lation of Utila in comparison with all other populations was

probably caused by adaptation to local environmental condi-

tions as well as intra-and interspecific (e.g. other anole lizard

species) competition (Schoener, 1969, 1970; Lister, 1975;

Dunham et al., 1978). These authors proposed that individuals

with larger body size have selective advantages on small islands

with strong intraspecific competition. Predation could also be

a possible driving force of body-size differentiation between

populations (Schoener, 1969, 1970; Lister, 1975; Dunham

et al., 1978). Further investigations are needed to address

factors that best explain the differentiation of Utila compared

with other populations.

Colonization of islands

According to the results of the assignment tests, the most likely

scenario of colonization turned out to be a mixture of

hypotheses A and B. The Cayos Cochinos possibly served as

stepping-stones for an independent migration to Utila and

Roatan, and Utila may have also been colonized directly from

the mainland. We found no evidence for direct migration

between Utila and Roatan. This scenario was supported by the

fact that only the Cayos Cochinos showed a strong connection

to the mainland, whereas Utila and Roatan demonstrated a

strong association to the Cayos Cochinos, but almost no

relationship to the mainland. Previous workers assumed that

Utila could additionally be colonized from the mainland. One

individual from Utila was assigned to the mainland, suggesting

that Utila could have been colonized from the mainland and

the Cayos Cochinos independently, but migration from the

Cayos Cochinos was much stronger.

The possibility of multidirectional migration (hypothesis

C) was rejected based on the results of the assignment tests.

But it is hard to see why the island populations of Utila/

Roatan showed such small genetic traces from the mainland,

despite the possibility of independent multiple migration

events within a continuous landscape, as assumed by

hypothesis C (island model). Migration was inferred to have

been limited to a strictly directional movement from the

mainland to the Cayos Cochinos, and from there independ-

ently to the islands Utila and Roatan. For example, we

detected no ancient migration routes from either Utila or

Roatan to the Cayos Cochinos (no individual from the Cayos

Cochinos was unambiguously assigned to Utila or Roatan),

whereas multiple individuals on both Utila and Roatan had

their origin on the Cayos Cochinos. Thus migration was

strongly unidirectional, which would be highly unlikely in a

continuous landscape. However, it should be mentioned that

in a continuous landscape source–sink populations from

prime to marginal habitat could lead to a similar pattern.

Currently we have no reason to assume that Utila and Roatan

belong to marginal habitats in a formerly continuous

4.0

6.0

8.0

10.0W

eigh

t (g)

Wei

ght (

g)

83

50

55

60

65

70

75

Siz

e (c

m)

Siz

e (c

m)

Utila Roatan Mainland CayosCochinos




50

55

60

65

70

75

80(a) (b)

(c) (d)

4

7669

3.0

4.0

5.0

6.0

7.0

8.0

Figure 3 Box plots for each variable depict

the median, 25th and 75th percentiles (box)

and whiskers extending an additional 1.5·;

outliers are indicated by open circles and

numbers of individuals. Differentiation

among species and populations in size (a,c)

and weight (b,d) separated by sex (a,b,

females; c,d males).



landscape. Consequently, we treated this interpretation of the

data as unlikely.

Hypothesis A proposed that N. bicaorum evolved on either

Utila or Roatan and subsequently colonized the other island.

This hypothesis could not definitely be rejected since the low

variance and genetic differentiation between these two islands

was compatible with this hypothesis. However, no individual

of Utila was assigned to Roatan or vice versa, thus results of

the assignment tests were inconsistent with this possibility.

An explanation for the similar genetic composition of these

two islands could be the fact that both were colonized

independently from the Cayos Cochinos as the source

population. In this case, the genetic similarity would be due

to ancient genetic similarity rather than to migration events

between these islands in the recent past. Morphologically, the

distinct character of both islands was accentuated by signi-

ficant differences in body size and weight. Thus assignment

tests were supported by morphological differentiation,

because migration should have weakened morphological

differentiation as well. It should be mentioned that strong

selection regimes in the presence of gene flow can result in

the same morphological pattern. However, as no evidence for

gene flow was found in assignment tests, this possibility is

unlikely.

Concerning ambiguous assignments, Cornuet et al. (1999)

pointed out that assignment/exclusion tests in GeneClass2

may show two types of error: type A errors where the correct

population is not listed; or type E errors where the correct

population is listed with additional possible populations. In

our study, all individuals were assigned to at least one of the

collected sample sites, and in doubtful cases the assignment

test tended to assign individuals to two or more populations

out of four, thus type A errors are assumed to play only a

minor role in this context. Type E errors were likely to be

responsible for ambiguous assignments, since some individuals

were assigned to more than one population with the same

probability (Table 5). This kind of error was likely in the case

of uncertainty in assignment of individuals from the Cayos

Cochinos to the mainland. We assume that assignment could

be further improved with a higher number of loci, as also

suggested by Cornuet et al. (1999).

ACKNOWLEDGEMENTS

We would like to acknowledge the essential help from

COHDEFOR (Corporacion Hondurena de Desarollo Fores-

tal), Tegucigalpa, Honduras and FUPNAPIB (Fundacion

Parque National de Pico Bonito) for providing collection

permits and helpful advice. We are grateful to Anne

Haberberger and Kai Schreiter for providing their data. We

are also indebted to workers from the IGUANA STATION/

Utila for field assistance and the leader of the station, Dr

Gunther Kohler (Natural History Museum and Research

Institute Senckenberg, Franfurt/M., Germany) for supporting

this study. We especially want to thank Stefan Hartel and

Michael Lattorff (Martin-Luther-Universitat Halle/S.) for

helpful laboratory advice. Additionally, we would like to

thank Dr Anja Schunke for statistical suggestions. We are

grateful to Dr Martin Haase and three anonymous reviewers

for constructive comments, which greatly improved the

manuscript. Lastly, we want to thank Dr Bradley Sinclair

for linguistic improvement of the manuscript.

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BIOSKETCHES

Cornelya Klutsch is a PhD student at the Molecular System-

atics Department of the Zoologische Forschungsmuseum

Alexander Koenig (ZFMK) and is primarily interested in

population genetics and biogeography at the population level.

Bernhard Misof is Curator in Entomology and head of the

Molecular Laboratory at the ZFMK. His research concentrates

on phylogenetic studies of a variety of organisms.

Wolf-Rudiger Grosse is working at the Department of

Zoology at the Martin-Luther-Universitat Halle/S. His research

focuses on taxonomic, ecological, conservation and biodiver-

sity studies in amphibians and reptiles.

Robin Moritz is a professor at the Department of Zoology at

the Martin-Luther-Universitat Halle/S. He is interested in all

aspects of molecular ecology, working mainly on evolutionary

processes in social systems.

Editor: Brett Riddle



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