Download Vive le difference! Sexual dimorphism and adaptive patterns in

272
Vive le difference! Sexual dimorphism and adaptive patterns in lizards of
the genus Anolis
Marguerite A. Butler1
Department of Zoology, University of Hawaii at Manoa, 2538 McCarthy Mall, Edmonson 152, Honolulu, HI 96822, USA
Synopsis The repeated, convergent evolution of body shape and microhabitat use in Greater Antillean lizards of the
genus Anolis (anoles) provides compelling evidence of the importance of microhabitat specialization in shaping
morphology. Interestingly, sexual dimorphism is also extensive, with males and females differing in body size as well as in
shape. It is important to note that the components of shape analyzed in these studies is related to locomotion and are
size-adjusted, including: relative limb and body lengths and mass of the body. Numbers of lamellae were also used and
these do not vary with size. Furthermore, dimorphism in both size and shape differs by habitat type. Thus, does
functionally-relevant sexual dimorphism imply that one sex is the ‘‘ecological’’ sex, with the other being maladapted to
it’s environment? Alternatively, sexual dimorphism may interact with adaptive diversification. Different classes of
individuals within a species may act as separate ecological units if they play ecologically different roles. Here, I reanalyze
a data set of morphological data for 15 species of Puerto Rican and Jamaican Anolis, which represent two largely
independent adaptive radiations of lizards. I test for concordance between size and shape dimorphism and microhabitat
(ecomorph) type, and for ‘‘parallel’’ patterns of sexual dimorphism among species. I integrate these results and, in the
light of previous research, evaluate the relative influence that larger-scale ecological patterns have on sexual dimorphism,
as well as the influence of sexual dimorphism on community structuring. I conclude that the presence of ecologicallyrelevant dimorphism may in fact increase the adaptive diversity present within a community.
Introduction
Is there any relationship between sexual variation,
interspecific variation, and the environment? Early
workers (Selander 1966; Schoener 1967; Emlen and
Oring 1977) recognized the importance of ecology
for the evolution of sexual dimorphism, especially as
it relates to one of three ultimate causes of sexual
dimorphism: differences in reproductive biology,
reducing competition between the sexes, or independent specializations of the sexes to a bimodal
distribution of resources (Slatkin 1984; Gaulin and
Sailer 1985; Shine 1989). However, this interest in
the role of extrinsic factors in the evolution of sexual
dimorphism has been largely eclipsed by the rise of
sexual selection in the evolutionary literature, which
has focused attention almost exclusively on withinspecies processes (Darwin 1871; Orians 1969; Trivers
1972; Stamps 1983; Zeh 1987; Bjorklund 1990; Pyron
1996; reviewed in Fairbairn 1997; Cox et al. 2003,
2007). While sexual selection can undoubtedly be a
potent selective force when it occurs (Andersson
1994), the loss of the greater hierarchical perspective
is unfortunate because there is no theoretical or
empirical justification to assume that the processes
which produce variation among species and between
sexes are decoupled.
Variation between the sexes has rarely been
considered in studies of adaptive radiation or
adaptive diversification in general (Liem 1974;
Losos 1992; Schluter and McPhail 1993). Most
studies have focused on one sex only (usually
males), or have pooled individuals regardless of
sex. However, there are at least three possible
relationships between sexual differences and interspecific variation. The same processes that generate
diversity between species may also produce diversity
between sexes. Such a relationship between morphology and the utilization of resources may be
quantitative and predictive, driven by one primary
functional relationship. For example, the head sizes
of carnivores may be matched to the size distribution
of prey, or larger lizards may use larger perches such
that there is a linear relationship between the width
of the perch and the size of the animal. In this case,
there is predicted to be a direct relationship between
sexual differences in resource utilization and sexual
From the symposium ‘‘Ecological Dimorphisms in Vertebrates: Proximate and Ultimate Causes’’ presented at the annual meeting of the Society
for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
1
E-mail: [email protected]
Integrative and Comparative Biology, volume 47, number 2, pp. 272–284
doi:10.1093/icb/icm061
Advanced Access publication June 25, 2007
ß The Author 2007. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
Sexual dimorphism and adaptation in Anolis
dimorphism (Dayan and Simberloff 1994).
Alternatively, niche partitioning may occur along
multiple dimensions, with sexes acting as independent ecological units and adopting different patterns
of resource utilization (Heatwole 1989). In this case,
the sexes and species will be differentiated morphologically, such that they cluster by ecological type,
but they will fit together as a complex jigsaw puzzle
in multiple dimensions. Thus, it may be difficult to
find a simple connection between sexual dimorphism
and ecological variation (see Fig. 1 for a simplified
visual representation of these alternatives). Because
of the multidimensional aspect of the problem,
the second alternative is more difficult to detect,
even though the underlying cause is a result of the
same ecological theory. The most obvious pattern in
this situation is that the sexes and species in this
community will cluster by ecological type and
show greater ‘‘niche packing.’’ Finally, interspecific
specialization may reflect adaptation to different
resources and intersexual specialization may reflect
differences in reproductive biology. The degree of
sexual dimorphism possible, however, may differ
under different distributions of resources. In this
case, particular habitats are predicted to promote
sexual differences.
Ecological context of anoles
Lizards of the genus Anolis are a particularly
appropriate group to investigate the interaction of
sexual and interspecific patterns. Anolis is an extremely diverse genus with over 300 species (Losos 1994).
Approximately half of the species are distributed in
the Caribbean, with the remainder in South and
Central America. Anoles share several general characteristics: they are small, arboreal, diurnal, insectivorous lizards. Species vary, however, in size and
shape of the body, degree of arboreality, prey size,
locomotion and foraging, and in social behavior.
Anolis is a classic example of adaptive radiation,
having experienced essentially independent radiations
on each of the islands of the Greater Antilles
(Cuba, Hispaniola, Jamaica, and Puerto Rico), in
each case producing a suite of species morphologically and behaviorally specialized in ways that use
different parts of the environment. For example,
species that occupy open habitats have long legs that
provide a great capacity for running and jumping.
In contrast, those species that specialize on twigs
have short legs that enhance maneuverability in
their narrow, irregular habitat. Moreover, the same
set of habitat specialists—termed ecomorphs and
named for the part of the habitat they use
273
Fig. 1 A graphic illustration of the parallel (or correlated)
niches hypothesis (A) versus independent niches (B).
An arrow connecting the means for males and those for
females in multivariate space will produce a set of parallel
vectors in (A) and vectors set at different angles in (B).
Note that since these are vectors, the slope as well as the
direction of the difference is important. For example, if the
positions of males and females reversed in one species, their
sexual dimorphism vector will be opposite in orientation to
the other species, even if slopes are the same. To simplify
presentation, only symbols representing the mean male and
female values for three species are presented. However, the
analyses presented in the text involve testing for differences
among ecomorphs, each represented by multiple species. The
axes are the morphological variables used in the analysis, possibly
after dimension-reduction by principal components or canonical
variates analysis (i.e., a form of multiple-group PCA).
(e.g., crown–giant, grass–bush, trunk–crown, trunk–
ground, and twig)—has evolved repeatedly across
the four islands (Williams 1983; Losos et al. 1998).
The different microhabitats that ecomorphs occupy
seem to favor different lifestyles. For example, grass–
bush anoles occupy small bushes or tall grass, which is
generally a thick matrix of thin perches near the
ground. They tend to have long hind limbs and short
forelimbs, are good jumpers, and use jumping quite
frequently to move about their habitat as well as
to capture prey (Moermond 1979; Losos 1990a).
274
In contrast, twig anoles have short limbs, live in the
canopy on the thin extremities of branches, and almost
exclusively walk rather than run or jump. Twig anoles
tend to be constantly moving about their habitat and
are the most actively foraging of all anoles. Trunk–
ground anoles, on the other hand, live on the broad,
open surfaces of the lower portions of tree trunks and
on the ground, and accordingly have long limbs.
Trunk–ground anoles are good runners and jumpers,
spend long periods essentially motionless in a perching
posture scanning their environs, and tend to run when
they do move. Trunk–ground anoles use the sit-andwait strategy of foraging more than do any other
Anolis.
Social behavior has been well-studied in a few
specie of Anolis. Their sterotypical mating system is
one of resource-defense polygyny. In most species
that have been studied, large males defend highquality territories that encompass smaller territories
of several females (Rand 1967a; Jenssen 1970; Stamps
1975; Trivers 1976; Schoener and Schoener 1980;
Stamps 1983; Jenssen 1995; Stamps et al. 1997).
Unlike many bird species, both males and females
may be territorial, although females generally have
small exclusive territories and larger home ranges
that they share with neighbors.
One species that lacks any degree of territoriality is
the twig anole Anolis valencienni, it also differs from
most other anoles in several other respects. The
presence of a large colorful throat structure (dewlap)
used for social signaling is a male-specific trait
in most other anoles. Both male and female
A. valencienni, however, possess large dewlaps
which they use frequently (Hicks and Trivers
1983). Additionally, whereas females of most anoles
are usually no longer receptive to males after mating
(Crews 1973), A. valencienni females have been
observed to copulate multiple times in one day
(Hicks and Trivers 1983) and even share a communal egg-laying site.
In addition, anoles vary considerably in the extent
of sexual dimorphism in body size (Schoener 1969;
Stamps 1983; Butler et al. 2000), ranging from
species in which the sexes are the same size to others
in which adult males are more than three times the
mass of adult females; the sexes also differ in
ecomorphologically-relevant proportions of various
parts of the body (Schoener 1967; Butler and Losos
2002). Similarly, sexual differentiation in microhabitat (Collette 1961; Rand 1967a, 1967b; Rand and
Rand 1967; Schoener 1967; Jenssen 1970; Andrews
1971; Schoener and Schoener 1971a, 1971b; Lister
1976, 1981; Scott et al. 1976; Talbot, 1979; Pounds
1988; Lister and Aguayo 1992; Powell and Russell
M. A. Butler
1992; Rodriquez Schettino and Martinez Reyes 1996;
Butler and Losos 2002), diet (Schoener 1967, 1968;
Schoener and Gorman 1968; Lister 1976; Talbot
1979; Floyd and Jenssen 1983; Preest 1994; Parmelee
and Guyer 1995; Perry 1996) and behavior is
substantial among West Indian anoles.
West Indian anoles thus contain extensive ecomorphological differentiation, both among species
that have radiated into specialized microhabitats on
each island and between sexes within these species.
In what follows, I analyze patterns of dimorphism in
size and shape, and combine these new analyses with
previous results in order to address the following
questions: Does sexual dimorphism in size and shape
suggest adaptation to microhabitat type? If adaptation is occurring, but males and females differ, can
sexual variation contribute to community-wide
diversity? Conversely, does the community within
which the species lives provide an important context
for the evolution of sex differences?
Methods
Data collection
I measured five morphological characters from adults
of both sexes of members of each ecomorph class on
Puerto Rico and Jamaica (sample sizes ¼ 3–29;
mean ¼ 16.4): mass, snout-to-vent length (SVL),
forelimb and hind limb length (FOREL and
HINDL), and numbers of sub-digital lamella on
the fourth toe of the hind foot (LAMN; lamellae are
laterally expanded scales on the subdigital toepads
used for clinging to inclined or vertical surfaces).
Localities are described by Butler and Losos (2002).
These two islands represent two independent adaptive radiations (Losos et al. 1998). I used the natural
logarithm of all variables; mass was first cube-root
transformed to place it on a linear scale with length
measurements. I used the geometric-mean method to
separate size and shape (Butler and Losos 2002),
with SIZE defined as the arithmetic mean of logadjusted SVL, MASS, FOREL, and HINDL (LAMN
is not included as it does not scale intraspecifically,
and only weakly interspecifically, with size).
Components of shape were calculated for each
individual by taking the difference of each logvariable with SIZE.
Mean values of the morphological measurements
for each species and sex were presented previously
(Butler et al. 2007). Previous comparative studies
established that both interspecific and intersexual
variation in these characters is adaptive with
respect to differences in habitat use (Locos 1990
b,c; Butler and Losos 2002).
275
Sexual dimorphism and adaptation in Anolis
Table 1 Results of morphological canonical variate analysis
Eigen value
Cumulative variance
Likelihood ratio
Approx. F-value
NumDF
DenDF
P-value
(A) Significance tests of canonical variate axes
CAN1
16.99
0.717
0.00234
56.68
116
1830
50.0001
CAN2
4.012
0.887
0.0421
30.93
84
1380
50.0001
CAN3
2.206
0.979
0.211
20.13
54
924
50.0001
CAN4
0.478
1.000
0.677
8.51
26
463
50.0001
(B) Canonical structure
Variable
Can1
Can2
Can3
Can4
Total
SSVL
0.863
0.450
0.155
0.171
SMASS
0.422
0.293
0.073
0.855
SFOREL
0.540
0.378
0.686
0.308
SHINDL
0.819
0.403
0.386
0.135
SLAMN
0.791
0.604
0.069
0.074
0.136
0.103
Between species-sex classes
SSVL
0.888
0.427
SMASS
0.593
0.380
0.0875
0.704
SFOREL
0.608
0.392
0.670
SHINDL
0.852
0.386
0.342
0.0820
SLAMN
0.816
0.573
0.0607
0.0446
0.261
0.427
0.203
Pooled within species-sex classes
SSVL
SMASS
0.616
0.608
0.137
0.181
SFOREL
0.252
0.334
0.758
0.0562
0.501
0.972
SHINDL
0.539
0.503
0.601
0.309
SLAMN
0.556
0.803
0.115
0.181
All species are of the genus Anolis. The morphological variables are size-adjusted (see below). Associated eigenvalues and significance levels of
canonical variate axes (A) followed by canonical structure (B: total, between group, and pooled within group loadings of shape morphology
variables on each canonical axis). Groups in this analysis were the species-sex classes.
NumDF ¼ numerator degrees of freedom; DenDF ¼ demoninator degrees of freedom; Can1–4 ¼ Canonical variate axes 1 through 4;
SVL ¼ snout-to-vent length (mm); MASS (g); FOREL ¼ forelimb length (mm); HINDL ¼ hindlimb length (mm); LAMN ¼ lamella number;
SIZE ¼ natural log of the geometric mean size; SSVL ¼ size-adjusted SVL ¼ log(SVL) – SIZE; ‘‘S’’ preceeding variable name indicates size-adjusted
variables, calculated in the same fashion as SSVL.
Multivariate analyses of shape dimorphism
I used analysis of variance (ANOVA) and multivariate analysis of variance (MANOVA) to test for
effects of sex, ecomorph type, their interaction,
and species nested within ecomorph type on shape
variation (Proc Reg and Proc GLM in the SAS
statistical language). Multiple comparisons were
controlled at an experiment-wise error rate of 5%
using the Tukey–Cramer method. The relative
importance of each factor or interaction was
estimated using components of partial variance
explained by each term in the model (Olejnik and
Algina 2000; Langerhans and DeWitt 2004) (partial
2; because they are partial variances, their sum can
exceed 100%). These analyses, including a phylogenetic version, was presented by Butler et al. (2007).
I used canonical variate analysis to reduce the
dimensionality of the multiple-group data. The
dependent variables were the measurements of shape
described earlier. The independent variables were the
species-sex classes (loadings are reported Table 1).
Correlated or independent niches
I tested the hypothesis of correlated differences
between the morphology of males and females
using MANOVA. If males and females have separate
niches, a plot of individual measurements in a
coordinate system with canonical variate scores as
axes should reveal that the male and female
276
observations form clusters. These clusters should be
grouped by sex and ecomorph type (here, species is a
replicate of ecomorph type).
If we draw a vector connecting the means of
males and females for each species, we can think of
our MANOVA as testing whether these male–female
(M–F) vectors differ across ecomorph types (Fig. 1).
In all cases, if males and females differ, the length
of the M–F difference vector is greater than zero. Thus,
when there are multiple species, differences in sexual
dimorphism among species may arise because either
they have differ in the lengths of their male-female
difference vector (i.e., the differ in the magnitude
of sexual dimorphism; Fig. 1A), or they differ in the
directions or angles of their M–F difference vector
(Fig. 1B). A MANOVA will find a significant
difference between sexes from either or both sources.
In order to separate the alternatives of sexual
dimorphism in magnitude or direction, we can
employ a simple trick by normalizing (i.e., artificially
equalizing) the magnitudes of the sex difference
vectors. Once we remove magnitude differences, any
differences that remain are from differences in
direction. Thus, if species vary by ecological type,
our test of correlated or independent niches comes
down to testing whether the vectors of the different
ecological types differ in length or direction (i.e., the
slopes of the lines), which can be accomplished by
two MANOVAs, one on the original data on shape
testing for magnitude þ direction, and the second
on the normalized data on shape testing for
direction only.
Thus, the difference vector between males and
females in canonical variate space defines the
magnitude and direction of multivariate dimorphism.
I tested whether ecomorphs differed in shape
dimorphism, both in magnitude and direction of
sexual dimorphism difference vectors. I used the
canonical variate scores as the dependent variables,
and ecomorph, sex, and the term species nested
within ecomorph, and the interaction between
ecomorph and sex as independent variables.
A significant ecomorph by sex interaction term
indicates that the M–F vector differs among ecomorphs (any difference in either magnitude or
direction). To clarify whether the difference can be
attributed to direction in addition to magnitude,
I also conducted the MANOVA after normalizing
the observations for males and females so that the
mean M–F vector would have the same length in each
species. In this case, a significant ecomorph by sex
interaction supports the hypothesis of independent
niches (Fig. 1B), whereas an insignificant interaction
supports the hypothesis of parallel niches (Fig. 1A).
M. A. Butler
Dimorphism in shape between ecomorphs and across
islands
I computed the distance between males and females
in shape (i.e., the magnitude of shape dimorphism;
also equivalent to the mean Mahalanobis distance
between males and female within a species). This is a
means of reducing the multivariate variation between
males and females within a species to a single
number. I then compared mean dimorphism in
shape across ecomorphs and islands and their
interaction. Incorporation of phylogenetic information into this analysis is not possible because
phylogenetic relationships and insular effects are for
the most part confounded.
Niche-filling analyses
The above analyses of shape dimorphism examine
patterns of differences between the sexes. An
important conceptual distinction is that although
sexual differences and ecological variation are
involved, by casting the problem in terms of sexual
dimorphism, what is compared is the extent to
which within species variation is affected by ecology
(i.e., whether some habitat types promote or
constrain dimorphism, or whether the form or
direction of dimorphism is different between habitat
types). In contrast, niche-filling analyses measure the
contribution of each sex to morphological diversity
at the community level, considering each sex as a
potentially independent ecological unit. Thus, conceptually, these analyses quantify the additional
contribution of sexual variation, above that of
(single-sex) interspecific variation, and consider
each sex relative to other groups within the
community, which may be of different sex, or of
either sex of a different species and ecomorph type.
Niche theory predicts that organisms will evolve
morphologies to match their ecological roles.
Thus, by convention, the ‘‘morphospace’’ is the
combination of possible morphologies in our set of
organisms, and can be represented by plotting the
organisms’ position along one or several morphological axes (Hutchinson 1957; MacArthur 1958).
Morphological diversity can then be assessed by
comparing the filling and overlap among groups in
morphospace.
I used individual canonical variate scores to test
hypotheses of morphospace filling. I binned individual observations into cubes of morphospace defined
by intervals of one canonical variate unit along
canonical variate axes one to three. I measured the
volume of morphospace occupied by male Anolis by
counting the number of cubes occupied by one or
Sexual dimorphism and adaptation in Anolis
277
more individuals. I then measured the increase in
volume attributable to adding females by counting
the number of additional cubes filled when females
were included. Significance was assessed by randomizing the sex of individuals within species using
20,000 permutations of the data. Code implementing
this test in the R statistical language is available
at the author’s website (http://www2.hawaii.edu/
mbutler/software.html). To account for any phylogenetic confounding, analyses were re-run after
eliminating the two species whose closest relatives
share the same ecomorph type (A. pulchellus and
A. stratulus). This test measures the amount by
which morphospace is expanded when females are
added to a male-only analysis and vice versa. These
analyses were presented by Butler et al. (2007), but
are partially reproduced here for comparison with
the above MANOVA analyses. Separate analyses of
niche-filling based on morphological data using an
alternate ordination method (Principal Components
Analysis, PCA), as well as niche-filling based
on ecological data were also previously presented
(Butler et al. 2007).
To visualize the position of the sexes and species
in morphological space, I plotted 20% contours of
the 3D kernel density using the ks package written in
the R statistical language (Duong 2005). The
densities were computed using kernel discriminant
analysis in three dimensions (using canonical variate
scores Can1–Can3) on ecomorph-sex groups.
The data entering into all analyses (both
MANOVA-based and nonparametric niche-filling)
were based on individual measurements, rather than
on species’ means. All ANOVA and MANOVA
analyses were performed in the SAS statistical
language.
Results
Both sexual dimorphism in size and shape have
strong associations with type of structural microhabitat, but not with phylogeny (Fig. 2; Butler et al.
2000; Butler and Losos 2002; Butler and King 2004).
Species of anoles using different microhabitats vary
greatly in shape in agreement with previous studies
(Fig. 3). Within species, the sexes differ in the same
morphological traits that distinguish the ecomorphs,
and for which the ecological significance of morphological variation is well-understood (Losos
1990b,c; Butler and Losos 2002): females have
relatively longer bodies and more lamellae in the
toepad than do males, whereas males have longer
limbs (Fig. 3). In addition, the extent and form of
dimorphism varies among the different ecomorph
Fig. 2 (A) A phylogenetic hypothesis for the species used in
this study (Butler et al. 2007). Ecomorph designations of species
are indicated, showing the multiple evolutionary transitions
between ecomorph (microhabitat specialist) types. (B) Sexual
dimorphism in size varies with ecomorph type (Butler et al.
2000). Trunk–crown and trunk–ground anoles have great
dimorphism in size while the remaining ecomorphs are less
dimorphic in size. (C) Dimorphism in shape was calculated as the
Mahalanobis distances between the sexes (see text). Crown giant
anoles have a high degree of dimorphism in shape, twig anoles
have less pronounced dimorphism, and the remaining are
intermediate.
278
M. A. Butler
Table 2 MANOVA results for dimorphism in shape and test of
parallel versus independent niches
Effect
Wilks’ k F-value P-value
p Qden r g2
Distance þ Angle
Sex
0.599
Ecomorph
0.00906
Ecomorph Sex
0.838
Species(Ecomorph) 0.135
78.78 50.0001 5
1
1 40%
328.84 50.0001 5
4
4 69%
5.35 50.0001 5
4
4
4%
31.04 50.0001 5 10
5 33%
39.63 50.0001 5
1 25%
Angle only
Sex
0.748
Ecomorph
0.00576
Ecomorph Sex
0.136
Species(Ecomorph) 0.931
1
395.90 50.0001 5
4
4 72%
30.87 50.0001 5
4
4 39%
2.14
0.0054 5 10
5
1%
‘‘Distance þ Angle’’ indicates the ordinary MANOVA results, whereas
the ‘‘Angle’’ refers to analyses of shape data after normalizing all
species to the same intersexual difference in distance. All shape
variables are entered into the model as dependent variables.
Independent variables included in the model are listed under ‘Effect’.
‘F-value’, value from F distribution; p, number of dependent variables;
Q, number of independent degrees of freedom; r, minimum of p or Q;
2, multivariate partial variance ¼ 1 1/r
Do males and females have independent niches?
Fig. 3 Characterization of shape dimorphism among the
ecomorphs (Butler et al. 2007). Relative means for
ecomorphs and sexes (white, females; grey, males) for
shape morphology variables (y-axes). Ecomorph-sex means
are adjusted for all other effects in the ANOVA models
(LSMEANS option in Proc GLM in the SAS statistical language;
see Methods section), and plotted relative to the grand
mean (centered at 0). Stars indicate significant sexual
differences within ecomorphs. Sexual dimorphism in body
length (SVL) occurs in ecomorphs with the shortest and
longest bodies, dimorphism in forelimbs in ecomorphs with
the longest forelimbs, and dimorphism in hind limbs in
ecomorphs with the longest hindlimbs. All ecomorphs are
dimorphic in lamella number, except twig anoles, which have
the greatest lamella numbers relative to body size.
types (Fig. 3). Ecomorphs that are highly dimorphic
in size, however, may not be highly in dimorphic in
shape (trunk–ground and trunk–crown anoles are
highly dimorphic in size but intermediate in shape;
the crown–giant anole is highly dimorphic in shape
but low in size), at least for the Puerto Rican and
Jamaican species (compare Fig. 1B, with Fig. 1C; see
also Butler and Losos 2002). Thus, dimorphism in
shape reveals a different ecological pattern than does
dimorphism in size.
MANOVA reveals that dimorphism in shape contributes substantially to morphological diversity
within anoles (Table 2, distance þ angle method),
with sex accounting for 40% of the partial variance
in total shape diversity and the interaction between
ecomorph and sex accounting for 69% of multivariate partial variance. Furthermore, the MANOVA
results support the hypothesis of independent niches.
Sexual dimorphism in shape is significantly different
whether we adjust for the magnitude of the
difference in shape or not (Table 2; all results have
P-values 50.0054). This indicates that the sexual
dimorphism in shape differs in both the magnitude
of the dimorphism as well as in the angle (indicating
that dimorphism in shape takes on different forms)
between different species and ecomorphs. These
effects are not reduced when phylogeny is taken
into account (Butler et al. 2007).
Analyses of packing in morphospace reveal that
sexual dimorphism is responsible for a large proportion of the total ecomorph niche space occupied.
As expected (based on previous studies), the ecomorphs occupy largely nonoverlapping portions of
multivariate morphological space. However, I demonstrate here that sexes within ecomorphs also occupy
unique regions of morphological space (Fig. 3, Table 3;
Butler et al. 2007). Only 14% of occupied cells in
morphological space contain both male and female
individuals. By contrast, females uniquely occupy
45% of morphospace and males uniquely occupy
279
Sexual dimorphism and adaptation in Anolis
Table 3 Morphospace niche-packing analysis
Both sexesa
Ecomorph
Nindb
Totcubes
Males
c
e
Uniquecubesd
Unique%
Females
Nind Totcubes Uniquecubes Unique% Nind Totcubes Uniquecubes Unique%
Trunk-ground 166
95
78
27
79
51
34
12
87
57
32
11
Trunk-crown
150
76
72
25
63
38
26
9
87
47
37
13
Crown-giant
31
29
21
7
16
16
12
4
15
13
9
3
Grass-bush
88
65
57
20
43
36
23
8
45
38
26
9
Twig
58
43
43
15
19
16
10
3
39
33
27
9
94
220
36
273
All
Total cubes
493
289
f
45
f
154
182
We compared the overlapping versus unique space occupied by ecomorphs and ecomorph-sex classes to assess the relative contributions to
morphospace volume.
a
‘Both sexes’ refers to ecomorph analyses with sexes combined, whereas ecomorph-females and ecomorph-males separates each ecomorph
class by sex.
b
Nind, number of individuals.
c
Totcubes, the number of (morphospace volume) cubes filled by each sex, ecomorph or ecomorph-sex class; these cubes may contain individuals
of more than one class. See Methods Section for details.
d
We measured uniquecubes, the volume occupied by each class. It is the volume of morphospace that is occupied solely by the given class relative
to the entire volume occupied by all classes. Uniquecubes excludes those cubes which contain more than one class.
e
‘Unique%’ refers to the percentage of Unique cubes occupied relative to the total number of cubes (289).
f
Forty-seven cubes are occupied by both sexes.
36% of morphospace. Thus, sexual dimorphism
significantly increases the density of morphospace
occupied by the anole radiations (P ¼ 0.0048): a 59%
increase if the morphospace volume of both sexes is
compared to that of only females, and an 88% increase
compared to the male-only volume. This result
remains significant when closely-related species of
the same ecomorph are not included (P ¼ 0.0018)
or if the analysis is repeated using principal
components analysis (P ¼ 0.017; Butler et al. 2007).
As with the MANOVA, the extent of intersexual divergence is a function of ecomorph
type (Table 3; Fig. 4): in some ecomorphs, sexes
appear to have more exclusive clusters, whereas in
others, the sexes form a mixed cluster. Trunk–crown
anoles, and especially trunk–ground anoles, have
more exclusive clusters. For example, male trunk–
ground anoles form exclusive clusters and insert
themselves in between clusters formed by female
trunk–ground anoles and crown–giant anoles
(Fig. 4B and C). These ecomorph-sex groups are
neighboring adjacent ecomorph types, and thus
behave as separate ecological units. The sexes
of the crown–giant, grass–bush, and twig anoles,
on the other hand, are more thoroughly interdigitated. Note that multiple species contribute to
an ecomorph, with each ecomorph independently
evolving on each island (with the exception of grass–
bush anoles, which are absent from Jamaica).
Thus, this analysis further demonstrates extreme
morphological convergence to niches associated
with habitat type.
Discussion
The meaning of sexual dimorphism and adaptation
A simple question has motivated my research on
sexual dimorphism in anoles. If morphology reflects
adaptation to the environment, but sexes differ in
morphology, what does this mean? Are females ‘‘less
adapted’’ than males? Do sexual differences in
habitat drive sexual dimorphism? Or do males and
females have ‘‘independent adaptations’’ to the
environment? If the latter is true, can there be a
‘‘female niche’’ and a ‘‘male niche’’ (‘‘econes’’ in the
terminology of Heatwole 1989) such that sexual
dimorphism interacts with adaptive diversification
such that sexual differences increase ‘‘species
packing’’?
Correlated or independent niches?
The finding here that niches of males and females
cannot be described simply as ‘‘parallel’’ (Fig. 1A)
corroborates the finding by Butler and Losos (2002)
that each sex is adapted to their respective microhabitats. If the differences in shape between the
sexes were simply parallel across all species, then it
would be possible to find a simple functional
relationship between shape and preferred habitat.
For example, a small increase in hind limb length
may result in a 1-cm increase in the diameter of
perch used. Thus, we find that males and females can
be better described as having ‘‘independent niches’’
(Fig. 1B). We know from previous work that neither
sex is maladapted, but, rather, interspecific analyses
280
M. A. Butler
Fig. 4 Three-dimensional visualization of morphological space (Butler et al. 2007). The plot is based on individual data with ecomorphs
(colors) and sexes (light ¼ females, dark ¼ males) indicated. Several species belong to each ecomorph type, thus part of the irregular
shape is a result of interspecific variation.Views (A) through (C) show different views of the same three-dimensional object.
281
Sexual dimorphism and adaptation in Anolis
show that each sex has strong multivariate correlations between shape and microhabitat (Butler and
Losos 2002). These correlations are simply slightly
different for each sex.
Are these differences between ecology and
morphology biologically significant? Does it imply
that there is some sex-specific functional demand?
Or is it something else? In the absence of functional
data, it appears that the fact that sexes differ may not
require special explanation related to sexual behavior.
Rather, the driving pattern may be how the species
and sexes fit within the community.
Niche-filling analyses
Macroevolutionary tests of niche filling often
describe the idea of ‘‘niche space’’ as a multidimensional hypervolume, with species occupying
different regions of morphospace. Thus, increasing
‘‘diversity’’ includes those analyses that add to the
morphospace on the periphery of the cluster, as well
as filling the gaps between ecological species such
that the niche space is more fully occupied.
Sexual dimorphism may increase the degree of
‘‘niche packing’’ if the sexes of different species are
interdigitated across the resource spectrum. This
hypothesis is not possible to test with standard
linear model or ANOVA-style analyses. If the
hypothesis is true, the clusters may pack together
in irregular ways. Moreover, what we really wish to
know is whether the sexes are filling unique space
that is left vacant by the other sex, and the classical
regression-based techniques cannot detect an increase
in the packing and filling of niche space. Butler
et al. (2007) devised a nonparametric niche filling
analysis.
If sexes are able to act as independent
‘‘ecospecies,’’ then sexual variation may increase
‘‘niche packing,’’ and ultimately, diversity at the
community-wide level. Indeed, analyses of morphospace packing reveal that sexual dimorphism is
responsible for a larger proportion of the total
ecomorph niche space occupied (Fig. 3; Butler et al.
2007). On an ecological scale, intersexual niche
packing implies that sexual variation may allow
greater biomass of Anolis per area of forest. Species
are often observed to expand their niche breadth in
the absence of competitors (i.e., ecological release,
reviewed in Dayan and Simberloff, 1994). If this
variation can be converted into sexual dimorphism
via disruptive selection, then it is possible to have
an interplay between interspecific and intersexual
variation. Thus, islands with younger faunas are
predicted to have greater sexual dimorphism, which
is gradually transferred to interspecific diversity as
faunal buildup progresses (Butler et al. 2007).
Sexual selection
Is it natural selection or sexual selection driving the
increase in morphological diversity? Differences
between the sexes in use of resources have been
documented in many species of Anolis. In previous
studies, I have found that intersexual differences in
habitat use are great and correlated with morphological dimorphism (Butler et al. 2000, 2007; Butler
and Losos 2002). In contrast to environmental
factors, sexual selection probably plays a lesser role
in driving the evolution of sexual dimorphism in
Anolis. Although sexual selection for large size in
males as a means of obtaining large territories, and
the females they contain, is commonly invoked as an
explanation for lizard sexual dimorphism (reviewed
by Stamps 1983), it is difficult to attribute the
patterns observed here to that cause. For example, in
those ecomorphs with significant dimorphism in
shape, males have lesser relative mass than do
females, shorter relative body length, and fewer
lamellae. If anything, this pattern is opposite to
what one might expect if the evolution of dimorphism is related to superior fighting ability in males.
Interestingly, the one pattern that is tightly
associated with the pattern of dimorphism in size
is whether sexes form more exclusive or mixed
clusters in morphospace. The trunk–ground and
trunk–crown ecomorphs with strongly sex-specific
clusters are those with the largest difference between
male and female body size (Fig. 2B; Butler et al.
2000), and may be the most territorial. However,
from the perspective of niche partitioning, it does
not matter which sex occupies which portion of the
resource space; all that matters is that they are
nonoverlapping. It should be equally likely that one
sex or the other occupy a particular niche. Indeed,
the sexes occupy roughly equal fractions of unique
morphospace in each ecomorph, whether sexes form
unique clusters or not (Fig. 4, Table 3). Thus, the
niche space attributable to each ecomorph is
similarly, and greatly, expanded whether sexual
selection is operating or not. For the evolution of
community-wide ecological diversity, sexual selection
does not matter.
It is possible, then, that sexual selection in this
morphological diversification simply biases the
occupation of a particular niche by one sex or the
other. The range of morphologies that can be
supported within the environment, and the extent
282
to which sexual selection is feasible, however, should
be determined by ecological opportunity.
Conclusion
Which is more important, interactions within species
(e.g., sexual selection), or interactions between
species (here, between sexes and species)? In the
case of Anolis, the influence of the environment is
pervasive. Ecological opportunity seems to set the
bounds for the ranges of morphologies that can
evolve, and there seems to be equal opportunity for
variation to be expressed between species of different
habitat types or sex-specifically. While ecology does
influence within-species patterns (i.e., ecological
patterns of dimorphism; MANOVA and ANOVA
results presented above), by far the largest
effect is in the packing and filling of morphospace
(Fig. 4, Table 3). Adding females to a male-only
analysis increases the volume of morphospace
occupied by 88%. Some of the differences between
sexes observed here are as great as if sexes formed
their own ecomorph (see especially trunk–ground
males and females in Fig. 4). This is truly an
impressive feat of evolutionary convergence, as
females are not clustering with conspecific males,
or even females of related species, but rather
distantly related females of the same ecological
type. Since there is no theoretical or empirical
reason to expect that processes which produce
variation among species and between sexes are
decoupled, perhaps we should not be surprised.
Perhaps the question should not be ‘‘why are the
sexes different,’’ but rather ‘‘why should the sexes be
the same?’’
Acknowledgments
I gratefully acknowledge Jonathan Losos for intellectual guidance, collaboration, and many stimulating discussions over the years. Jim Cheverud
provided the idea for the vector-based analysis of
correlated versus independent niches using
MANOVA. Without the tireless field assistance of
Ling-ru Chu, C. K. Wang, and Jeff Higa, this work
would not have been possible. A belated thank you
to my dissertation committee at Washington
University, who provided stimulating guidance:
Stanley Sawyer, Owen Sexton, Jane Phillips-Conroy,
Bob Sussman, Alan Templeton, JC, and JBL. I thank
Tarn Duong, Stanley Sawyer, and Aaron King for
advice on analyses and Bob Cox, Hal Heatwole, and
an anonymous reviewer for critical comments which
greatly improved the manuscript. This work was
supported by a grant from the National Science
M. A. Butler
Foundation, the Society for the Study of Amphibians
and Reptiles. I received support in the field from the
Discovery Bay Marine Laboratory, Jamaica and
the El Verde Field Station, Puerto Rico. Thank you
also to the symposium organizers for the invitation
to participate in this symposium.
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