Oecologia (2016) 181:885–894
DOI 10.1007/s00442-016-3618-1
POPULATION ECOLOGY – ORIGINAL RESEARCH
Ecological and evolutionary influences on body size and shape
in the Galápagos marine iguana (Amblyrhynchus cristatus)
Ylenia Chiari1 · Scott Glaberman1 · Pedro Tarroso2 · Adalgisa Caccone3 ·
Julien Claude4 Received: 27 August 2014 / Accepted: 17 March 2016 / Published online: 4 April 2016
© Springer-Verlag Berlin Heidelberg 2016
Abstract Oceanic islands are often inhabited by endemic
species that have undergone substantial morphological
evolutionary change due to processes of multiple colonizations from various source populations, dispersal, and local
adaptation. Galápagos marine iguanas are an example of
an island endemic exhibiting high morphological diversity,
including substantial body size variation among populations and sexes, but the causes and magnitude of this variation are not well understood. We obtained morphological
measurements from marine iguanas throughout their distribution range. These data were combined with genetic and
local environmental data from each population to investigate the effects of evolutionary history and environmental
conditions on body size and shape variation and sexual
dimorphism. Our results indicate that body size and shape
are highly variable among populations. Sea surface temperature and island perimeter, but not evolutionary history
Communicated by Jean-François Le Galliard.
Electronic supplementary material The online version of this
article (doi:10.1007/s00442-016-3618-1) contains supplementary
material, which is available to authorized users.
* Ylenia Chiari
[email protected]
1
Department of Biology, University of South Alabama, 5871
USA Drive North, Mobile, AL 36688, USA
2
CIBIO/InBIO, Centro de Investigação em Biodiversidade
e Recursos Genéticos da Universidade do Porto, Campus
Agrário de Vairão, 4485‑661 Vairão, Portugal
3
Department of Ecology and Evolutionary Biology, Yale
University, New Haven, CT 06520, USA
4
Institut des Sciences de l’Evolution, UMR 5554, CNRS/IRD/
UM/EPHE, Université de Montpellier II, 2 Place Eugène
Bataillon, 34095 Montpellier Cedex 5, France
as depicted by phylogeographic patterns in this species,
explain variation in body size among populations. Conversely, evolutionary history, but not environmental parameters or island size, was found to influence variation in
body shape among populations. Finally, in all populations
except one, we found strong sexual dimorphism in body
size and shape in which males are larger, with higher heads
than females, while females have longer heads than males.
Differences among populations suggest that plasticity and/
or genetic adaptation may shape body size and shape variation in marine iguanas. This study will help target future
investigations to address the contribution of plasticity versus genetic adaptation on size and shape variation in marine
iguanas.
Keywords Ecomorphology · Islands · Phenotypic
evolution · Reptiles · Sexual dimorphism
Introduction
Islands have long been recognized as natural laboratories
for the study of evolution (e.g., Darwin 1859; Mayr 1967)
due to their restricted geographic boundaries, generally
small size, and often traceable geologic history. Oceanic
islands of volcanic origin, in particular, are well suited for
uncovering patterns and processes of ecological diversification since they emerge as empty spaces available to be colonized by organisms, whereas mainland systems are generally saturated by diversified and structured communities
(e.g., Gübitz et al. 2005; Losos and Ricklefs 2009). Morphological traits are among the best-studied characters that
have been used to understand patterns and causes of variation on islands. Large morphological variation can occur on
islands as a consequence of the exploitation of free niches
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886
in the newly colonized environment or from multiple distinct colonization events from diverse source populations
(e.g., Van Valen 1965; Schluter and Grant 1984; Robichaux
et al. 1990; Gillespie et al. 1997; Losos et al. 1998; Millien 2006; Losos and Ricklefs 2009; but see also Bolnick
et al. 2007). The Galápagos archipelago, which consists
of 19 major islands located approximately 960 km from
the mainland (Snell et al. 1996), is among the best-known
examples of volcanic islands with organisms exhibiting
high levels of morphological variation (e.g., Parent et al.
2008). This archipelago has a relatively well-known geologic history, aiding studies of the patterns and processes
of island colonization and ecological and morphological
diversification (e.g., Grant and Grant 2002; Parent et al.
2008; Ali and Aitchison 2014).
The marine iguana, Amblyrhynchus cristatus, is one of
the endemic organisms inhabiting the Galápagos. This species diverged from its sister group, the terrestrial iguanas
of the genus Conolophus, approximately 8.25 million years
ago. Divergence among currently existing marine iguana
populations dates at less than 50,000 years (MacLeod
et al. 2015). Molecular data suggest that the colonization
of existing islands went from east to west, from older to
younger islands of the archipelago, followed by some episodes of gene flow after populations were established on
different islands (Steinfartz et al. 2009).
Morphological studies conducted on a few populations
of marine iguanas have highlighted the existence of a wide
range of body size variation in this species. Body size
appears to be quite plastic in these animals, and changes
in body length have been observed during periods of food
shortage. For example, during El Niño events, marine iguanas may shrink in body length within just a few months
(Wikelski and Thom 2000). Body size variation in marine
iguanas has been attributed to natural selection—including
trade-offs between thermoregulation, food intake, and optimal food digestion—and sexual selection (e.g., Wikelski
and Trillmich 1994, 1997; Wikelski 2005). Marine iguanas possess a lek mating system, with a tight clustering of
males defending small territories and attracting females
(Wikelski et al. 1996, 2001). It has been suggested that
maximum achieved body size reflects a balance between
attracting mates and thermoregulatory and digestive performance (Wikelski and Trillmich 1997; Wikelski 2005). The
extent of body size variation across the species distribution,
however, is largely unknown, as is the impact of evolutionary history on this variation. Furthermore, the magnitude
and causes of body shape variation are not well understood.
Body shape variation may be functionally important for fitness-related activities and behaviors, as observed for other
lizards (e.g., Garland and Losos 1994; Losos and Miles
2002; Herrel et al. 2008; Kaliontzopoulou et al. 2012;
Scharf and Meiri 2013).
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The evolutionary history and ecology of marine iguanas
have been studied for many populations, permitting investigation of the factors influencing morphological variation
in this species. Examination of correlations between evolutionary history, environmental conditions, and phenotypic
variation has been used successfully in other organisms
to understand the contribution of these factors to morphological variation and evolution within and among species (e.g., Malhotra and Thorpe 2000; Chiari et al. 2004,
2009). Building on previous studies of body size variation
conducted on only a few marine iguana populations (e.g.,
Wikelski and Trillmich 1994, 1997), we assess the geographic patterns and environmental parameters influencing body size and shape variation on this species across its
entire distribution. Furthermore, we evaluate the influence
of evolutionary history, based on previously described phylogeographic patterns of marine iguanas from across the
archipelago (Steinfartz et al. 2009), on morphological variation (size and shape). We also tested whether variation in
morphology could be related to different environments. Our
hypothesis is that body size is mostly dependent on local
factors such as island perimeter (possibly related to food
availability, see below) and environmental conditions (e.g.,
temperature and productivity), and not strongly dependent
on evolutionary history. This would support previous indications that body size variation in marine iguanas is plastic (Wikelski and Thom 2000) and temperature dependent
(Wikelski 2005; Walters and Hassall 2006). Conversely, as
there is currently no indication that mating, feeding strategy, or locomotion differ among localities and therefore
show local adaptations, we predict a stronger relationship
between evolutionary history, genetic divergence, and
shape variation among populations, suggesting little influence of plasticity on shape. Finally, due to the lek mating
system of this species, we expect to find sexual dimorphism
in both size and shape to occur.
Materials and methods
Samples
Fieldwork was carried out in the Galápagos Islands in
1993. Sampling localities were recorded as global positioning system coordinates and included 16 sampling sites
(henceforth referred to as “populations”) across 12 islands
(Fig. 1; Supplementary material S1).
We only considered adults in this study, i.e., individuals for which sex could be positively identified based on
external morphology (Dellinger and von Hegel 1990).
Eight morphological variables were obtained with a calliper and a tape ruler, which included: snout-vent length
(SVL); tail length (TL); length of the front limb (LP);
Oecologia (2016) 181:885–894
887
Fig. 1 Map of the Galápagos
Islands with populations and
mitochondrial clades indicated
(modified from Steinfartz et al.
2009). Population abbreviations
(EPC, FMO, FPE, FPM, GCA,
ICW, IPA, MBN, PCI, PDL,
SCC, SFN, SFS, SJB, SRL,
SRP) are as in Supplementary
material S1
length of the third digit of the manus (LD); height, length
and width of the head (HH, HL, and HW, respectively); and
jaw length (JL) (Supplementary material S2). These variables are commonly sampled in lizards for morphological
and functional studies, as SVL, TL, LP, and LD are known
to be correlated with locomotor performance, while HH,
HL, HW, and JL are involved in feeding, courtship, and
mating (e.g., Vleck et al. 1981; Garland and Losos 1994;
Miles et al. 1995; Wikelski and Trillmich 1997; Wikelski
and Thom 2000; Losos and Miles 2002; Kaliontzopoulou
et al. 2012; Gomes et al. 2016). Furthermore, in marine
iguanas, the fingers of the manus are important for gripping
to resist waves and breaking surf while feeding on rocks
on the shore and intertidal zone (Y. C. and S. G., personal
observation)
Genetic data for all individuals, including mitochondrial
(D-loop) sequences and genotype data for 13 microsatellite
loci, were obtained from Steinfartz et al. (2009). Each individual was previously assigned to one of three mitochondrial clades (A, B, or C) by Steinfartz et al. (2009) based
on D-loop sequence data (Fig. 1; Supplementary material
S1); these clade assignments were also used in the current
analysis. We used both D-loop DNA sequences and microsatellite loci because they reflect distinct evolutionary time
frames, due to differences in coalescence times (Avise
2000). In this study, we examined only individuals for
which both genetic (mitochondrial and/or microsatellite)
and morphological data were available (Supplementary
material S1). For the morphological analyses alone, and for
the morphological and mitochondrial DNA data, we used
343 individuals, while 347 individuals were used for the
comparison of morphological and microsatellite data.
Morphometric and genetic analyses
All morphometric analyses were run in R version 3.0.1 (R
Core Team 2013). Analyses were run on size and shape
independently. Size and shape information were extracted
from linear measurements using the log-shape ratio
approach described in Mosimann (1970). Following this
approach, size was estimated as the geometric mean from
all the measurements of each individual, while shape corresponded to the log-shape ratio (here indicated simply as
“log-shape”) of linear measurements on size (Mosimann
1970). Mosimann’s approach avoids arbitrary choices of
which variables should represent size and is the best available method to accurately depict variation in size and shape,
especially when individuals of similar shape have different
sizes and vice versa (Jungers et al. 1995). The use of log
data allows linearizing relationships with covariables and
to easily analyze the presence of allometries—the relationship between changes in shape due to changes in size during growth. The use of the geometric mean helps account
for the fact that size information is carried by every linear
measurement. Due to the way they are calculated, log-shape
ratios could not be considered independent. Therefore,
prior to running the multivariate explanatory analyses on
shape data, we performed a principal component analysis
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888
on log-shape to remove the last null component of variation
(Claude 2008, 2013). In addition, the effect of explanatory
variables was also assessed on every single log-shape ratio
to identify which parts of shape were affected (see below)
(Claude 2008, 2013).
Congruence in how individuals are grouped by morphology (log-size and principal components of log-shape),
genetics (microsatellite loci), geography (geographic coordinates), or a combination of these (Supplementary material S3) was tested using the program Geneland version
4.0.0 (Guillot et al. 2012) in R. Geneland uses a Bayesian
approach to detect if individuals can be grouped based on
similarity in the data, and how many clusters (groups) of
individuals occur, without having a priori information on the
data. Datasets were run with ten independent runs, uncorrelated allele frequencies, maximum rate of Poisson process set to one hundred, 106 iterations, and thinning of 100.
When analyses included geographic coordinates, we used
an uncertainty in the coordinates of 0.02 degrees [about
2-km coastline, which corresponds to the approximate maximum migration estimate of marine iguanas (Lanterbecq
et al. 2010)] to account for individual dispersal.
To test for differences in size among populations, sexes,
and mitochondrial clades, a three-way ANOVA was run
on log-size data using the F-test and type II sum of squares
with population, sex, and mitochondrial clade as factors [factors are unbalanced within each category (Chiari et al. 2009;
Claude 2013)]. To estimate possible differences in sexual size
dimorphism among mitochondrial clades and populations,
the interactions between factors were also taken into account.
Differences in shape between populations, sexes, and
mitochondrial clades taking into account effects due to
allometric growth (relationship between log-shape and logsize) were estimated through a multifactorial multivariate
analysis of covariance using type II sum of squares and
products of the seven non-null PCs shape variables, with
population, sex, and mitochondrial clades as factors and
log-size as covariate. To estimate possible differences in
sexual shape dimorphism among mitochondrial clades and
populations, the interactions between factors was also taken
into account. To test for differences among populations and
sexes for each log-shape ratio, the effect of the explanatory variables was also assessed on every single log-shape
ratio alone. In these analyses, effects may be nested (e.g.,
clades within populations; Supplementary material S1). In
this case, the df for analyses with nested and interaction
effects take into account that some combinations of categories are absent in our sample design (e.g., missing one or
two clades for some populations; Supplementary material
S1). To test for differences in pairwise comparisons among
mitochondrial clades and sexes for each log-shape ratio a
Tukey test was run with mitochondrial clades and sex as
factors.
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Oecologia (2016) 181:885–894
Environmental data
To analyze the relationship between environmental parameters and size and shape variation among populations, we
obtained oceanic data on intertidal productivity estimated
from chlorophyll a concentration (mg m−3) and sea surface
temperature (SST; °C) from moderate resolution imaging
spectroradiometer data in the NASA Ocean Color site (oceancolor.gsfc.nasa.gov/) representing the period between
2000 and 2011, since data for the sampling year (1993)
were not available. Although we did not have images of
the year of sampling (low satellite coverage was available
in 1993), we assumed that a decade of data would adequately represent the overall temporal and spatial pattern
(see “Results”). We used chlorophyll a concentration as an
indicator of algal productivity among populations because
it is directly linked to marine iguana feeding requirements
since they primarily eat algae (Drent et al. 1999). We used
SST instead of deep-water temperature since marine iguanas feed and utilize the marine environment near the shore,
in the intertidal and subtidal zones (Trillmich and Trillmich
1986). Often, marine iguanas feed with most of their bodies
just barely covered by sea water (Y. C. and S. G., personal
observation). Although males may swim to deeper water to
feed, they typically stay within a few meters depth; therefore SST can be considered a good proxy for the water temperature experienced by marine iguanas, while sea depth
would not be representative of the habitat experienced
by these animals. We also obtained average monthly land
data on precipitation (mm), and minimum, maximum and
mean air temperature (°C) from WorldClim, which compiles weather station data from the period between 1960
and 1990 (Hijmans et al. 2005). The value for each sample
location was assumed to be represented by the nearest pixel
with a 2.5 arcmin spatial resolution (~4 km) for all variables. Remote sensing allows obtaining images of different
wavelengths for specific times and localities. These data
were related to variables of interest such as chlorophyll a.
In situ validation of the resulting data is frequently updated
(Werdell et al. 2003). ANOVA was used to assess whether
the variation at each environmental parameter among populations followed the same trend over time, with population
and year as factors. Island perimeter (m), which represents
the coastline and therefore the actual space mostly used by
marine iguanas, was measured from coastline geographic
information system data (global self-consistent, hierarchical, high-resolution geography database; www.ngdc.noaa.
gov/mgg/shorelines/gshhs.html) that was previously transformed to the Albers equal-area projection.
We ran a correlation analysis and a bivariate regression with population mean values for each environmental parameter calculated across the monthly or yearly
time spans versus the population mean log-size and mean
Oecologia (2016) 181:885–894
889
Results
log-size (independently of sex) occurred on Genovesa
(GCA; log-size = 4.1), while the largest mean log-sizes
were found in populations from Fernandina (FPE), Isabela
(ICW and IPA), Floreana (FMO), and San Cristóbal (SRL
and SRP) (Supplementary material S4). Sexual size dimorphism occurred in all populations (Table 1) except Genovesa (GCA), with the most pronounced size difference
between males and females occurring in one of the populations from Isabela (ICW) (Fig. 2; Supplementary material
S4). Although males were generally bigger than females
(Fig. 2; Supplementary material S4), the degree of sexual
size dimorphism differed among populations (Table 1).
ANOVA results indicated that the three major mitochondrial clades previously described for marine iguanas
(Steinfartz et al. 2009) did not explain log-size variation and
sexual size dimorphism (Table 1). When Geneland was run
with log-size data only, four clusters were recovered that
did not correspond to any geographic grouping of sampling
localities or to the microsatellite data clusters (11) previously identified by Steinfartz et al. (2009) and confirmed
here (Supplementary material S3), indicating that individuals within specific populations or microsatellite clusters
were not more similar in log-size than between populations
or microsatellite groups. Only individuals from Genovesa
(GCA) formed a distinct size group, while the remaining
three clusters comprised individuals from multiple populations (Supplementary material S3). When Geneland was
run on log-size data taking into account microsatellite data,
the clustering was similar to that obtained with microsatellite data alone (Supplementary material S3). When Geneland was run on log-size data taking into account geographic
coordinates or using genetic data and geographic coordinates together, the results were unreliable, as different numbers of clusters were obtained for the different runs, suggesting a lack of convergence of these runs (data not shown).
Size variation
Shape variation
Mean log-size differed significantly among populations
(Table 1; Supplementary material S4). The smallest mean
Mean log-shape differed significantly across populations, sexes (i.e., sexual dimorphism), and mitochondrial
Fig. 2 Box plot of size (not log transformed) considering the distinct
populations and each sex separately. Horizontal black bar represents
median value; whiskers represent most extreme values (maximum
and minimum values). Populations are ordered from the maximum to
the minimum body size and indicated with abbreviations as in Supplementary material S1. For each population the box plot on the left
represents males and the box plot on the right corresponds to females
log-shape and mean log-size and mean log-shape of
females and males separately. We also ran a regression
between island perimeter and chlorophyll a to estimate if
resource productivity may be correlated to island perimeter.
Regressions were run in R using t-test statistics (H0 = no
relationship) and two-sided p-value estimates.
Table 1 Influence of
population (Pop.), sex, and
mitochondrial clade, and their
interactions, to explain variation
in mean log-size in Galápagos
marine iguanas
Effect
Sum of squares
df
Mean square
F-value
p-value
Pop.
15
7.197
0.480
57.231
<0.001**
Sex
1
3.799
3.799
453.148
2
15
0.011
0.592
0.005
0.039
0.641
4.706
<0.001**
0.528
3
2
1
0.007
0.013
0.009
0.002
0.007
0.009
0.273
0.794
1.122
303
2.540
0.008
Clade
Pop. × sex
Pop. × clade
Sex × clade
Pop. × sex × clade
Residuals
<0.001**
0.845
0.453
0.290
Statistically significant p-values in italic
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Table 2 Mean log-shape
differences taking into account
sex, population (Pop.),
mitochondrial clade and
allometries (Log-size) as factors
Oecologia (2016) 181:885–894
Effect
Pillai
df
Approx. F
df num.
df den.
p-value
Sex
1
0.15815
6.951
7
259
<0.001**
Pop.
15
2.16786
7.926
105
1855
<0.001**
Clade
2
0.10549
2.068
14
520
0.012*
log-size
1
0.44767
29.989
7
259
Sex × pop.
Clade × pop.
Sex × Clade
Sex × log-size
Pop × log-size
15
3
2
1
15
0.39018
0.11752
0.03532
0.02894
0.51675
1.043
1.520
0.668
1.103
1.408
105
21
14
7
105
1855
783
520
259
1855
<0.001**
0.367
0.063
0.807
0.362
Clade × log-size
Sex × clade × pop.
Sex × pop. × log-size
2
1
15
0.04887
0.02354
0.46617
14
0.892
1.260
14
7
105
520
259
1855
2
1
1
0.05514
0.01646
0.02129
1.053
0.619
0.805
14
7
7
520
259
259
Sex × clade × log-size
Clade × pop. × log-size
Sex × clade × pop. × log-size
Error term
0.005*
0.526
0.513
0.042*
0.399
0.740
0.584
265
Approx. Approximate, num. numerator, den. denominator
Statistically significant p-values in italic
clades (Table 2; Supplementary material S5). Shape allometries—defined as changes in shape relative to changes in
size—occurred and differed among populations (Table 2)
and among sexes in distinct populations (Table 2). Each
log-shape ratio differed significantly among populations
(Supplementary material S5), with differences in shape
allometries among populations only occurring for LP and
HL (Supplementary material S5). Mitochondrial clades
differed significantly in LP (Supplementary material S5),
with individuals from clades C and A having the longest and shortest legs, respectively (data not shown). There
was a significant interaction between mitochondrial clade
and population, suggesting that evolutionary history, as
defined by the phylogeographic distribution of the three
mitochondrial clades, may not be the main factor influencing variation in LP among populations (Supplementary
material S5). SVL and head measurements (HH, HL; Supplementary material S5) differed among sexes, indicating
sexual dimorphism. According to the results of the Tukey
test, females have longer heads than males across populations (p-value = 0.0003, data not shown), while males
have higher heads than females (p-value < 0.0001, data not
shown).
When individual log-shape data were analyzed alone to
look for possible structure in how individuals are grouped,
six clusters were obtained in Geneland, with individuals
in each cluster being distributed across multiple populations and only individuals from Genovesa (GCA) forming
a single group distinct from the rest (Supplementary material S3). When microsatellite data were included in the
Geneland analysis, clustering was primarily determined by
13
microsatellite data structure, as shown by the correspondence between microsatellite clustering alone and the pattern obtained by analyzing log-shape data and microsatellites together (Supplementary material S3). Results on the
influence of sampling locality (geographic coordinates) on
log-shape could not be obtained due to a lack of convergence of the runs in Geneland (data not shown).
Influence of environmental parameters on size
and shape variation
With the exception of chlorophyll a, the environmental parameters considered in this study generally showed
a similar trend of variation among populations across the
12-year period or across months over a 30-year period.
ANOVA interactions of year/month and population were
not significant except for chlorophyll a (p-value <0.001,
data not shown). These results suggest that environmental
data exhibit consistent patterns across years and that the
lack of environmental data for the particular year of morphological and genetic sampling for this study should not
bias the results, as it is unlikely that there would be large
variation in these parameters among the populations over
the study period. We found no relationship between population values of chlorophyll a and island size (data not
shown).
We found a significant negative relationship between
mean log-size variation among populations and SST, and
a positive relationship with island perimeter (Table 3). SST
and island perimeter were also negatively and positively
correlated, respectively, to mean log-size variation across
Oecologia (2016) 181:885–894
populations in both females and males (Table 3). No significant relationship was observed between mean log-size
and any other environmental parameter considered in these
analyses (Table 3). We did not observe any significant relationship between log-shape or log-shape for females and
males analyzed separately and any of the environmental
parameters or island size (data not shown).
Discussion
Size and shape variation
In animals, heat loss is proportional to the surface area to
volume ratio, with larger organisms having a smaller ratio
and thus reduced heat loss. On this physical basis, many
ecological rules have been proposed to explain the relationship between body size and external temperature. Marine
iguanas, like all reptiles, are ectotherms; thus, their body
temperature depends on the external climate. In ectotherms
in particular, a relationship between variation in body size
and temperature (temperature-size rule) has been proposed,
with colder temperatures leading to an increase in body
size (Angilletta and Dunham 2003; Walters and Hassall
2006 and references therein; Kingsolver and Huey 2008).
Our results reveal significant body size variation among
populations of Galapágos marine iguanas, which is not
correlated to evolutionary history (i.e., genetic divergence
in microsatellites or phylogeographic patterns based on
mitochondrial DNA) among populations. This supports
previous indications that body size in marine iguanas may
be highly plastic (Wikelski and Thom 2000). Mean body
size is found to be influenced by SST and island perimeter. For adult marine iguanas, which do not have natural
predators and for whom aggressive inter-specific competition is largely absent, maximum body size is mainly
constrained by the amount of algal pasture available, the
time spent feeding, and thermoregulation (Wikelski and
Carbone 2004). Our results, based on a larger sample size
and a more widespread sampling than previous work (e.g.,
Wikelski and Carbone 2004), support the importance of
thermoregulation, but not productivity, in influencing mean
body size in this species.
Marine iguanas feed on algae either in the intertidal costal area or by swimming and diving into the cold oceanic
water offshore to feed on submerged algae (Drent et al.
1999). Although energy expenditure between these two
foraging modes is similar (Drent et al. 1999), the warming
up rates can be quite different, thereby influencing foraging and digestive efficiency (Wikelski and Carbone 2004).
The observed relationship between SST and mean body size
suggests that temperature may constrain body size in these
animals by determining the time an animal can spend in the
891
Table 3 Pearson correlation coefficient and correlation analysis
between population mean log-size, population mean log-size per sex
and environmental parameters
Correlation
SST—Size
SST—SizeM
SST—SizeF
Chloro.—Size
Chloro.—SizeM
Chloro.—SizeF
Prec.—Size
Prec.—SizeM
Prec.—SizeF
Tmean—Size
Tmean—SizeM
Tmean—SizeF
Tmax.—Size
−0.5751
−0.5828
−0.5455
0.3494
0.3884
0.2924
−0.0185
−0.0420
0.0547
−0.1359
−0.0521
0.0097
−0.2194
t-test
−2.63
−2.68
p-value
0.0198*
0.0178*
−2.44
0.0289*
0.185
0.137
0.272
0.946
0.877
0.841
0.8938
0.848
0.972
0.4142
0.3768
0.5131
0.396
0.4211
0.313
1.40
1.58
1.14
−0.07
−0.16
0.20
−0.14
−0.20
0.04
−0.84
Tmax.—SizeM
Tmax.—SizeF
Tmin.—Size
Tmin.—SizeM
Tmin.—SizeF
IslPer.—Size
−0.2370
−0.1765
0.2280
0.2163
0.2693
0.5189
−0.91
−0.67
0.88
0.83
1.04
2.27
0.0394*
IslPer.—SizeM
0.5117
2.23
0.0427*
IslPer.—SizeF
0.6093
2.88
0.0122*
SST Sea surface temperature, SizeM male mean body log-size, SizeF
female mean body log-size, Chloro. chlorophyll, Prec. precipitation,
Tmean mean temperature, Tmax. maximum temperature, Tmin. minimum temperature, IslPer. island perimeter
Statistically significant p-values in italic (df always 14)
water feeding, either in the intertidal area or in the offshore
waters. Because larger body mass corresponds to decreased
body surface area to volume ratio, larger individuals are generally less sensitive to heat loss (e.g., Pincheira-Donoso et al.
2008). Therefore, having a larger body size and mass may
allow marine iguanas to be less sensitive to heat loss due to
exposure to cold water during underwater feeding, where
food is more abundant, or in localities where water is colder.
Although the results presented here indicate a role for
thermoregulation in influencing mean body size in marine
iguanas, it is also possible that colder waters may be more
productive and may harbor more abundant and higher quality food, which would enable individuals to grow larger. In
this study, we used chlorophyll a as a measure of productivity, but future work could examine other measures (e.g.,
algal height or type of algae) to further test the relationship
between food availability, temperature, and body size. It is
also plausible that the association between island perimeter and body size found in this study may be related to the
number of sites available for feeding, and thus related to
the amount of algal pasture available.
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892
It is also possible that differences in longevity among
populations may explain some of the variation in mean size
between sampling localities, as populations with older, and
thus larger, individuals may have higher mean size than
populations with younger, smaller individuals. There are
no basic data available on age structure and longevity of
marine iguanas across the archipelago to test this question
directly. However, marine iguanas, like reptiles in general,
experience indeterminate growth, so that once sexual maturity is reached, growth slows down and largely depends on
available resources. Since we only sampled adults in our
study, observed size differences are not expected to be a
function of age, but rather available resources.
Our results indicate that populations of marine iguanas
differ both in mean shape and at each of the morphological
variables analyzed. Mitochondrial clades, but not microsatellite loci grouping, are associated with variation in shape
and leg length. This could suggest that evolutionary history,
more than recent population differentiation (as depicted
by microsatellites), has influenced shape variation across
populations. In contrast to what was observed for size variation among populations, environmental parameters do not
have an effect on shape, suggesting that local adaptation for
shape variables may not have occurred.
Size and shape sexual dimorphism
Size and shape sexual dimorphism occur in all populations, with size sexual dimorphism differing among populations. Males are larger than females on all islands except
Genovesa. Adaptive plasticity and/or genetic adaptation of
sexual size dimorphism may therefore occur in this species.
These results confirm previous work on a small number
of populations (e.g., Wikelski and Trillmich 1997). Both
natural and sexual selection are likely to influence sexual
size dimorphism in these animals (Wikelski et al. 1996;
Wikelski and Trillmich 1997; Wikelski and Romero 2003).
Larger male size would offer an advantage during male
fighting for territory and positioning in the lek. In addition, larger males are favored for mating (Wikelski et al.
1996), with male mating success highly skewed toward a
few successful males due to female choice (Wikelski et al.
2001). Females generally mate with the males showing
more active mating behavior (Wikelski et al. 1996, 2001).
However, larger males would also be more sensitive to food
availability (size-dependent mortality), requiring a larger
amount of food overall (Wikelski and Trillmich 1997).
Mean body shape and individual morphological variables also differ between the two sexes. Males have higher
and shorter heads than females. These traits could be associated with head use in male–male competition and mating
behavior (e.g., Herrel et al. 2001; Scharf and Meiri 2013).
Mating behavior involves lek formations, with the most
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Oecologia (2016) 181:885–894
attractive males occupying the center of the lek, and consists of active male–male fights with head-push or headbob interactions with competing males and head-bobs or
copulation attempts with females (Wikelski et al. 2001;
Partecke et al. 2002).
Conclusion
Our results indicate that body size and shape differ among
populations of marine iguanas. Variation in mean body
size among the study locations is correlated with SST and
island perimeter. Variation in body shape among populations could instead be partially explained by evolutionary
history as depicted by species phylogeography. Sexual
dimorphism occurs in all populations except one, Genovesa. Future work should address the influence of plasticity versus adaptation in relationship to the observed differences in body size and shape among sex, location, and
island. In particular, our results indicate that Genovesa may
represent a unique system among the Galapágos islands
and that local adaptation may be occurring for body size
and shape on this island. Studies focusing on the possible
association between island size, population size, individual
competition for basking sites, and distance among lekking
groups could provide further understanding of the observed
differences in body size among populations. Ecological
and behavioral work will help address whether differences
in body shape among populations may be associated with
diverse functional performance (e.g., swimming, gripping
onto rocks), different population densities, mating behavior, or diverse habitats.
Acknowledgments All the experiments comply with the current
laws of the country in which the experiments were performed. Sampling permits to obtain the data used for this work have been published elsewhere (Rassmann 1996; Steinfartz et al. 2009). We are
thankful to K. Rassmann and S. Steinfartz for sharing morphological
and microsatellite data used in this work and for comments on an earlier version of this manuscript. We are thankful to several reviewers of
this article for their useful comments.
Author contribution statement Y. C. and S. G. conceived the
study. S. G. collected the molecular data in A. C.’s lab. Y. C. and J. C.
discussed and planned the morphometric analyses. P. T. collected the
environmental data. Y. C. performed all the analyses. Y. C. wrote the
article; S. G. refined it; J. C., P. T., and A. C. provided comments.
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