2009 Blackwell Verlag GmbH

Accepted on 8 April 2009

J Zool Syst Evol Res doi: 10.1111/j.1439-0469.2009.00531.x

1
Programa de Doutorado em Ciencias Ambientais, Universidade Federal de Goias, Goias, Brazil; 2Laboratorio de Ecologia teorica e
sntese, Universidade Federal de Goias, Goias, Brazil; 3Departamento de Biologia Geral, Universidade Federal de Goias, Jata,
Goias, Brazil

Phylogenetic autocorrelation and heritability of geographic range size, shape and

position of ddler crabs, genus Uca (Crustacea, Decapoda)
J. C. Nabout1,2, L. C. Terribile2,3, L. M. Bini2 and J. A. F. Diniz-Filho2

Abstract
The aim of this study was to evaluate the levels of phylogenetic heritability of the geographical range size, shape and position for 88 species of
ddler crabs of the world, using phylogenetic comparative methods and simulation procedures to evaluate their t to the neutral model of
Brownian motion. The geographical range maps were compiled from literature, and range size was based on the entire length of coastline
occupied by each species, and the position of each range was calculated as its latitudinal and longitudinal midpoint. The range shape of each
species was based in fractal dimension (box-counting technique). The evolutionary patterns in the geographical range metrics were explored by
phylogenetic correlograms using Morans I autocorrelation coecients, autoregressive method (ARM) and phylogenetic eigenvector regression
(PVR). The correlograms were compared with those obtained by simulations of Brownian motion processes across phylogenies. The distribution
of geographical range size of ddler crabs is right-skewed and weak phylogenetic autocorrelation was observed. On the other hand, there was a
strong phylogenetic pattern in the position of the range (mainly along longitudinal axis). Indeed, the ARM and PVR evidenced, respectively, that
ca. 86% and 91% of the longitudinal midpoint could be explained by phylogenetic relationships among the species. The strong longitudinal
phylogenetic pattern may be due to vicariant allopatric speciation and geographically structured cladogenesis in the group. The traits analysed
(geographical range size and position) did not follow a Brownian motion process, thus suggesting that both adaptive ecological and evolutionary
processes must be invoked to explain their dynamics, not following a simple neutral inheritance in the ddler-crab evolution.
Key words: Geographic range size shape position phylogenetic autocorrelation

Introduction
Geographic range is a pivotal and complex variable that has
been extensively studied in macroecology and conservation
biology (Brown and Lomolino 1998; Maurer 1999; Gaston 2003;
Holt 2003). Moreover, the geographical range can be described
by its size, form and position, and each of these characteristics
can oer dierent insights into the ecological and evolutionary
processes driving inter-specic variation in species ranges
(Bohning-Gaese et al. 2006). Nonetheless, the geographic range
size has received more attention in the literature. For example,
geographic range size is related to population density and body
size in a complex way and, consequently, is also associated with
extinction probability (Jones et al. 2005; Bohning-Gaese et al.
2006). Despite these considerations, we still lack a full understanding of the ecological and evolutionary processes related to
many characteristics of range dynamics (Gaston 2003).
The geographic range of a species likely reects the
inuences of phylogenetic constraints, limiting environmental
factors and dispersalextinction dynamics (species-specic
sensu Bohning-Gaese et al. 2006; Brown et al. 1996; Gaston
2003). Moreover, the size, shape and position of geographic
ranges are not constant through evolutionary time (Liow and
Stenseth 2007), and some recent studies have suggested that
geographical range size is heritable, because geographic ranges
of pairs of related taxa tend to be more similar than would be
expected by chance (Jablonski 1987; Hunt et al. 2005).
Conversely, other studies did not nd any evidence that
ranges size are heritable (Diniz-Filho and Torres 2002; Webb
Corresponding author: Joao Carlos Nabout (naboutjc@hotmail.com)
Contributing authors: Levi Carina Terribile (levicarina@unb.br), Luis
Maur cio Bini (bini@icb.ufg.br), Jose Alexandre Felizola Diniz-Filho
(diniz@icb.ufg.br)

J Zool Syst Evol Res (2010) 48(2), 102108

and Gaston 2003, 2005; Mouillot and Gaston 2007). Also, up

to this time, it is not clear which method is the best for testing
range size heritability (Hunt et al. 2005; Waldron 2007).
Further, we are not aware of studies focusing on the
heritability of species geographic shape and positions. The
shape of species ranges present great variation (Brown et al.
1996) and is determined by dierent physiographic aspects
(Ruggiero 2001). The range shape of coastal organisms, for
instance, are likely products of the coastline structure, whereas
the positions of geographic range along the coastline are
inuenced by environmental and dispersal constraints (Gaston
and Blackburn 2000).
Assuming that speciation processes are predominantly allopatric (Rosenzweig 1995; Losos and Glor 2003), we would
expect that ranges characteristics of related species are more
similar than would be expected by chance, reecting both
conservatism of ecological niche characteristics and dispersal
abilities. The heritability of range properties can be tested by
evaluating the level of phylogenetic dependency among species
and many papers have used dierent (albeit related) approaches
derived from comparative methods (Jablonski 1987; DinizFilho and Torres 2002; Bohning-Gaese et al. 2006). The use of
modern comparative methods in ecological research has
increased in the last 20 years because of the large amount of
phylogenetic information made available and due to computational and statistical advances (Pagel 1999; Martins 2000; DinizFilho and Torres 2002). For instance, phylogenetic autocorrelation analysis allows us to describe the phylogenetic structure
of data and provides a quantitative way to evaluate the
relationship between phenotypic similarity and phylogenetic
relatedness (Diniz-Filho 2001). Thus, it can be useful to
investigate patterns of geographic range heritability and niche
conservatism by comparing observed species divergence with

Phylogenetic autocorrelation and heritability of Uca

expectations from dierent evolutionary models. In this context, Brownian motion is one of several statistical models that
have been proposed to t comparative data and simulate their
evolution. Most importantly, Brownian motion has been used
as a neutral model in phenotypic evolution, describing changes
by random genetic drift, mutation-drift balance, or directional
selection in rapidly and randomly changing environments
(Felsenstein 1988; Hansen and Martins 1996; Diniz-Filho 2001).
In this study, we quantied attributes of geographic range
(size, shape and position) of ddler crabs (genus Uca) with the
aim to evaluate the levels of phylogenetic signal in these
attributes using phylogenetic comparative methods and simulation procedures (Brownian motion). Finding high levels of
geographic range size heritability has important implications.
First, this result could be associated with dierences in species
biological traits, which are related with variation in geographical range size across species. If geographic range size is traitdependent, we could expect that the other factors, besides
stochasticity, are relevant in shaping species range size
distributions. Second, in studies of correlated evolution
between traits, if there is a signicant level of dependence
among species trait values due to their phylogenetic relatedness, some sort of statistical control of Type I error rate is
needed (Felsenstein 1988). Finally, supposing a strong phylogenetic signal, we could predict the geographic range of species
of conservation concern from those of close relatives (Mouillot
and Gaston 2007 and reference therein).

Materials and Methods

Data
The genus Uca has a worldwide distribution, and is characterized by
strong sexual dimorphism and male asymmetry (Rosenberg 2001).
There are currently nine subgenera of ddler crabs, allocated to two
groups: narrow-front and broad-front. We measured geographical
range size and position for 88 species of ddler crabs of the world
(genus Uca), compiled from Crane (1975). The total geographical
range size (length) was measured in kilometers following the irregularities of the coast lines occupied by the species. The position of each
range was dened by its latitudinal and longitudinal midpoint.
Actually, there are 97 extant species currently recognized for the
genus Uca. However, the 88 species included in this study are
representative of the main clades of the group, and thus the exclusion
of nine species is not expected to qualitatively aect the overall
conclusions of a phylogenetic comparative analysis (Rosenberg 2001).
The geographic range shape was estimated by fractal dimension
analysis of occupied coastline. The fractal dimension is frequently used
in ecology and it is applied to measure the degree of complexity and
shape of environments (e.g. Halley et al. 2004; Thomaz et al. 2008).
We used the box-counting technique (Maurer 1994) to estimate the
fractal dimension (D) of each species. We use a regular grid of boxes of
variable side-length s superimposed over the species ranges, and the
boxes occupied, N(s), was counted. We repeated this process by
increasing s (the size of the boxes used here, in decimal degrees, were
0.5, 1, 2, 4, 8, 10), and the fractal dimension for each species range was
determined by the slope of log N(s) against log(1s).
The phylogenetic relationships among the 88 species of ddler crabs
were established by Rosenberg (2001), based on 236 morphological
characters. We used two phylogenetic trees constructed by Rosenberg
(2001) to generate the phylogenetic distance matrices used in this
study. The phylogeny A is the strict consensus tree of the eight mostparsimonious trees (length = 1.5385, Consistency Index = 0.158,
Retention Index = 0.655) from a maximum parsimony analysis
in paup 4.0b3a software (Sinauer Associates, Sunderland, MA,
USA). The phylogeny B is the strict consensus tree of 12 mostparsimonious trees (length = 1.517, Consistency Index = 0.161,
Retention Index = 0.66) built by constraining the set of species to

103
t into three distinct clades: the Indo-Pacic species, the American
crown species and the basal American species (see details in Rosenberg
2001). Branch lengths are not available for these two phylogenetic
trees, so our analyses must be interpreted as reecting mainly the
topological relationships among species and, thus, assuming roughly
constant evolutionary rates of divergence among them.
Despite the fact that the phylogeny is greatly based on morphological traits, this is by far the most complete phylogeny available for the
entire genus. Moreover, recent analyses support the idea that some
changes in the phylogenetic structure would have small qualitative
impacts on the results of comparative analyses using phylogenetic
autocorrelation (Diniz-Filho and Nabout 2009).

Phylogenetic comparative analyses

The phylogenetic patterns in the size, shape and position of geographic
ranges were initially explored by autocorrelation analysis, based on the
two phylogenetic trees. Phylogenetic correlograms were constructed
using Morans I autocorrelation coecients (Sokal and Oden 1978)
estimated at ve equal phylogenetic distance classes (Bininda-Emonds
and Gittleman 2000; Diniz-Filho 2001). Thus, the rst distance class
contains most of the variation at lower taxonomic levels, whereas the
last distance class contains the divergence among higher clades of the
group. Morans I at each phylogenetic distance class was given as:

"

 #
n  P P yi  y yj  y wij
i
j
I
P
S
y 2
i y i  
where n is the number of species; yi and yj are the values of the trait in
the species i and j; y is the average of y; wij is the element of the matrix
W, which assumes a value of one if the species pair i, j is within the
distance class interval. S is the count of these connections among
species in each W matrix for each class interval. Each Morans value
was tested for signicance using 999 permutations (Legendre and
Legendre 1998). The signicance of the entire correlograms was
established using the Bonferronis criterion, so that a correlogram can
be considered signicant if one of its Morans coecients is signicant
at the ak level, where a is the probability of type I error (generally
0.05) and k is the number of distance classes. The phylogenetic
correlograms for range size, shape and position were calculated using
the Spatial Analysis in Macroecology (sam; Rangel et al. 2006)
program.
Brownian motion evolutionary processes tracking the topological
relationships among species dened for each phylogenetic tree were
simulated 300 times in the pdsimul routine of the Phenotypic Diversity
Analysis Program (pdap program) (Garland et al. 1993). The pdsimul
initially estimates the mean value of the trait in the root of the
phylogeny, and produces the evolution of this trait using the model of
evolution (Brownian motion in this case). In Brownian motion, the
change of trait occurs independently in each lineage after the
speciation events, with no restrictions on the direction and relative
magnitude of the changes in time continuum (thus simulating genetic
drift).
The observed correlograms (geographic range size, shape, longitudinal and latitudinal) and Brownian correlogram were compared using
linear regression approach. The linear regression between Morans I
and phylogenetic distance class were calculated for the correlograms
from each simulation (Brownian motion). The angular coecient
distribution of linear regression was compared of angular coecient
obtained of linear regression among Morans I and phylogenetic
distance class of range size, shape, latitude and longitude.
We also evaluated phylogenetic patterns in geographic range
properties by using the autoregressive method (ARM; see Cheverud
et al. 1985). The autoregressive model is given by

y pWy e
where y is the vector containing the trait of interest, p is the
autoregressive coecient,  is residual term, and W is the weighting
matrix expressing the pairwise phylogenetic relationships among
species and thus analogous to the one used above for Morans I.

J Zool Syst Evol Res (2010) 48(2), 102108

 2009 Blackwell Verlag GmbH

104

Nabout, Terribile, Bini and Diniz-Filho

However, in this case the matrix W reects the relationship across the
entire phylogeny and was dened by the inverse of phylogenetic
distances among species, D, so that

1
W a
Dij
where alpha is a coecient that aects the non-linearity of the
relationship between phylogenetic distances and weighting. High
values of alpha, thus, indicate that only very closely related species
are similar to each other, and changing these alpha values can improve
the t of autoregressive model (Gittleman and Kot 1990). We selected
the best autoregressive model by searching alpha values that minimize
the Akaike Information Criterion (AIC; see Burnham and Anderson
2002) of ARM model. The coecient of determination (r2) of the
ARM model estimates the amount of variation in the trait of interest
(e.g. range size) that is explained by the phylogeny (phylogenetic
inertia or signal) (Cheverud et al. 1985). We used the sam (Rangel
et al. 2006) program to calculate the best ARM.
We also used the Phylogenetic Eigenvector Regression (PVR) to
estimate the phylogenetic signal in range properties (Diniz-Filho et al.
1998). The basic idea of PVR is to perform a principal coordinate
analysis of the D matrix and use the eigenvectors as predictors in a
multiple regression against species traits (in this case, geographic range
properties) (see Diniz-Filho et al. 2007 for a recent application in
macroecology). We extracted the eigenvectors from the two distance
matrices (one from each phylogeny) and selected which ones should be
used in the multiple regression by an exhaustive search using AIC (see
Diniz-Filho and Nabout 2009). As in ARM, the coecient of
determination (r2) of this multiple regression model estimates the
amount of phylogenetic signal in species traits.

Results
Among the 88 ddler crabs species analysed in this study, Uca
tetragonon has the largest geographic range size (85413.31 km;
Table 1), whereas U. tallanica has the smallest one (225.11 km;
Table 1). In addition to the wide variation in geographic range
size, its statistical distribution is strongly right-skewed, with
most of the species (ca. 60%) having ranges smaller than
10 000 km (Fig. 1).
For both phylogenies utilized, correlograms estimated for
geographic range position (mainly longitude) revealed signicant phylogenetic autocorrelation patterns, with closely related
species occurring at similar positions in species and distantly
related species occurring far apart in geographical space
(Table 2). Indeed, a simple correlation between geographic
distances (calculated based on species range latitudinal and
longitudinal midpoints) and phylogenetic distances yielded
signicant values for both phylogeny (r = 0.5248;
p = <0.001, for phylogeny A and r = 0.4106; p = <0.001
for phylogeny B, based on Mantel tests with 5000 random
permutations). On the other hand, the range size presented weak
phylogenetic signal, and only the Morans I for the rst distance
class was statistically signicant. The geographical range shape
(fractal dimension D) also presented weak phylogenetic signal
and no signicant autocorrelation coecient was detected even
for rst distance class (both phylogenies) (Table 2).
Correlograms from the simulated Brownian motion process
showed a clear monotonic decrease in Morans I coecients with
increasing distances in time, so that the observed correlograms
(range size, shape, latitude and longitude) suggested markedly
deviations from what would be expected if these properties have
evolved under a Brownian motion model. The distribution of
angular coecient obtained from regression among phylogenetic distance class and Moran I for each simulation (Brownian
J Zool Syst Evol Res (2010) 48(2), 102108
 2009 Blackwell Verlag GmbH

Table 1. Geographical range size (km) and range position (midpoint)

of 88 species of ddler crabs
Species
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca

thayeri
umbratila
ecuadoriensis
vocator
marguerita
galapagensis
herradurensis
rapax
virens
burguersi
mordax
pugnax
panacea
pugilator
subcylindrica
zacae
minax
brevifrons
uruguayensis
batuenta
saltitanta
tenuipedis
speciosa
spinicarpa
cumulata
beebei
deichmanni
limicola
leptodactyla
latimanus
panamensis
terpsichores
dorotheae
stenodactylus
inaequalis
oerstedi
tallanica
tomentosa
festae
coloradensis
crenulata
chlorophthalmus
crassipes
inversa
sindensis
argillicola
bengali
triangularis
annulipes
lactea
mjoebergi
perplexa
arcuata
forcipata
rosea
coarctata
ammula
urvillei
demani
typhoni
capricornis
paradussumieri
rhizophorae
dussumieri
bellator
hirsutimanos
longidigitum
polita

Range size Range shape Longitude Latitude

28311.51
3324.19
8914.57
18082.72
1204.14
3900.94
2564.58
32800.96
4114.87
30744.84
11736.64
6068.46
5043.03
10932.54
1338.60
4204.63
8347.41
5846.06
3558.15
5259.69
3294.90
5059.51
2790.28
4558.12
9366.59
5318.09
1130.69
2744.58
14740.09
9989.99
5046.17
4629.10
2817.85
7913.49
4642.99
2727.88
225.11
5200.71
4622.34
1051.71
4779.40
10979.55
46653.94
16672.73
3309.88
3628.55
10062.92
65045.43
64178.82
7345.33
7316.84
53452.58
13111.05
16730.41
12722.31
40768.94
10623.09
14056.21
10974.65
6760.52
7678.82
25405.99
986.39
52638.24
19606.42
7573.04
2780.61
11287.86

1.19
1.01
0.99
1.09
0.82
0.88
0.91
1.17
0.97
1.22
1.07
1.06
1.07
1.19
0.82
0.96
1.15
1.01
1.08
0.95
1.00
1.02
0.88
1.03
1.12
0.98
0.81
0.92
1.11
1.03
1.02
0.94
0.95
0.98
1.03
0.97
0.39
0.98
0.93
1.02
1.13
1.06
1.10
1.08
1.03
1.04
1.10
1.34
1.16
1.02
0.99
1.29
1.07
1.14
1.09
1.15
1.07
0.98
1.25
1.30
1.02
1.17
0.75
1.26
1.32
1.00
0.90
1.06

)65.50
)82.41
)91.29
)72.28
)95.65
)81.66
)83.50
)66.89
)93.60
)66.50
)65.72
)76.34
)92.93
)77.44
)97.05
)96.22
)83.09
)94.11
)50.47
)81.64
)82.13
)81.41
)85.26
)93.41
)61.23
)81.85
)79.08
)83.25
)65.15
)95.34
)81.43
)81.66
)79.02
)79.03
)80.86
)83.06
)80.75
)81.61
)81.61
)112.92
)113.39
42.19
139.68
43.48
56.13
)81.08
94.13
125.94
76.25
126.97
127.67
121.74
124.06
109.80
95.47
128.58
130.89
51.29
120.81
123.13
129.60
107.45
108.13
125.30
118.14
131.47
150.00
136.13

9.67
9.22
12.67
12.53
20.35
)1.13
10.02
9.70
26.50
9.97
10.40
36.63
26.15
31.03
26.05
16.33
32.99
15.34
)29.41
6.05
9.13
5.54
24.40
25.93
9.52
5.88
8.08
9.88
10.23
15.48
5.68
7.07
1.98
)2.16
5.21
9.86
)3.75
5.90
7.08
29.58
28.37
)16.44
1.76
0.48
27.16
7.50
8.27
)1.41
5.68
29.70
)14.67
)0.61
30.22
2.59
11.85
)1.89
)11.79
)5.31
)1.24
12.10
)15.79
8.40
1.88
)3.53
4.92
)15.03
)22.36
)16.89

Phylogenetic autocorrelation and heritability of Uca

105

Table 1. Continued
Species
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca
Uca

seismella
signata
elegans
borealis
dampieri
neocultrimana
hesperiae
vocans
vomeris
tetragonon
formosensis
heteropleura
intermedia
insignis
maracoani
ornata
stylifera
major
princeps
tangeri

Discussion
Range size Range shape Longitude Latitude
10949.37
9588.93
7775.01
2871.07
6880.42
23430.94
16443.94
52849.33
13804.30
85413.31
691.37
4814.91
911.70
4822.75
11361.05
5120.02
5421.38
15199.37
10216.21
13087.20

1.06
1.06
1.06
0.94
1.05
1.01
0.94
1.32
1.06
1.15
0.78
1.01
0.97
1.02
1.09
0.98
1.01
1.18
1.03
1.02

136.78
138.86
124.78
118.40
126.54
148.84
67.25
111.82
153.19
114.00
120.79
)80.87
)77.75
)80.93
)44.51
)81.43
)81.37
)69.85
)93.36
)12.89

)16.44
)15.95
)17.11
24.90
)15.90
)5.48
1.60
5.28
)12.55
0.37
23.93
5.35
6.50
5.33
2.96
5.94
5.78
15.34
13.50
8.69

Fig. 1. Frequency distributions of range sizes (km) for ddler crabs of

the world

motion) for phylogeny A vary from )0.06 to )0.40 and for

phylogeny B vary from )0.03 to )0.40. However, for both
phylogenies, the angular coecients of the observed correlograms were registered in tail of slope distribution (Fig. 2). The
slope for longitude was larger than slopes expected under
Brownian motion, indicating that correlogram for longitudinal
midpoint is steeper than expected by neutral evolution and that
closely related species are then more similar (i.e. have higher
Morans I in the rst distance class) than expected by Brownian
motion, tending to remain closer along longitudinal dimensional
than expected by chance alone. On the other hand, whereas the
slopes for latitude, range size and range shape were smaller than
slopes expected under Brownian motion, as expected by the
absence of phylogenetic pattern in these traits.
The ARM and PVR indicated similar results (Table 3). In
both phylogenies, a high fraction of the variance in the
longitudinal midpoint of the range was explained by phylogenetic relationships among species. On the other hand, geographic range shapes were not correlated with phylogeny.

The geographic range is a fundamental variable for studies in

macroecology and conservation biology. A search in ThomsonISI (Web of Science) using the terms geographic* range* in
the title, between 1991 and 2007, yielded 291 papers. Most of
these papers focused on the spatial patterns and determinants
of geographic range sizes (e.g. Oliers et al. 2004; Gross 2006;
Hawkins and Diniz-Filho 2006), while only a few have focused
on the heritability of range sizes (e.g. Hunt et al. 2005; Webb
and Gaston 2005; Waldron 2007).
Many of the papers discussing the subject of geographic
range size heritability reached conicting results (Webb and
Gaston 2003; Hunt et al. 2005). Here we expanded these
previous analyses and used dierent comparative methods
(phylogenetic correlograms, ARM and PVR) to estimate the
level of phylogenetic heritability in geographic range attributes (size, shape and position) of the worldwide distributed
genus Uca. All these methods showed congruent results and
demonstrated that the position of the geographic range
(especially longitudinal midpoint) showed a strong phylogenetic pattern.
The phylogenetic pattern in the longitudinal midpoint
provides support for the macroevolutionary patterns of diversication in ddler crabs which were previously proposed
(Rosenberg 2001). Currently, there are two alternative hypotheses about the diversication pattern of ddler crabs. The rst
hypothesis suggests that the basal narrow-front species arose in
the Indo-West Pacic (these early crabs splitted into multiple
narrow-front lineages and one broad-front lineage), and one
group dispersed to America and West Africa through the Bering
Strait, or also by island hopping across the tropical Pacic.
Later, the American broad-front taxa migrated back to the
Indo-West Pacic via the same route, generating the current
distribution of the group (Crane 1975). Salmon and Zucker
(1988), however, proposed an alternative hypothesis, where all
ddler crabs (including both broad- and narrow-front species)
lived near the Tethys Sea in the late Oligocene, and later
subdivided into American and Indo-West Pacic groups. These
authors suggested that the similarity of species in the dierent
groups (American and Indo-West Pacic) resulted from parallel
evolution and not a shared phylogenetic history. Moreover,
other studies using molecular phylogenies of 24 species of ddler
crab (Levinton et al. 1996; Sturmbauer et al.1996) do not
support Cranes hypothesis (centre of origin in the Indo-West
Pacic). Thus, in both hypotheses about ddler crab diversication, the trend toward longitudinal diversication is more
pronounced, explaining the strong relationship between phylogeny and the longitudinal midpoint by a sequential process of
vicariant allopatric speciation (Losos and Glor 2003). In ddler
crabs, this speciation process is highlighted mainly because some
events as, for instance, the closure of Tethys Ocean and the
expansion of the Pacic Ocean produced the barrier that
separated the American and Indo-west pacic species. The rise
of the Isthmus of Panama also separated ddler crabs species of
Eastern and Western America.
Conversely, the geographic range shape, size and latitudinal
midpoint had a much weaker phylogenetic pattern. Some
studies have detected weak phylogenetic patterns for range
size in mammals, shes, birds and parrots, using phylogenetic
correlograms (Diniz-Filho and Torres 2002; Freckleton et al.
2002; Blackburn et al. 2004; Jones et al. 2005; Bohning-Gaese
et al. 2006). Therefore, we concur with previous studies that
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106

Nabout, Terribile, Bini and Diniz-Filho

Table 2. Phylogenetic correlograms for geographic range size, geographic range shape (fractal) geographic position (latitude and longitude) and
Brownian motion in the 88 species of ddler crabs, using Morans I coefcients estimated at ve distance classes and signicance (Bonferroni
criterion p < 0.01)

Class
Phylogeny A
1
2
3
4
5
Phylogeny B
1
2
3
4
5

Brownian motion,
Morans I (%)

Range size,
Morans I
(p-value)

Range shape,
Morans I
(p-value)

Longitude,
Morans I
(p-value)

Latitude,
Morans I
(p-value)

0.746
0.549
0.310
0.084
)0.128

(99.33)
(96.33)
(74.33)
(49.66)
(4.33)

0.202
0.085
0.072
0.253
)0.091

(0.035)
(0.195)
(0.142)
(<0.001)
(<0.001)

0.088 (0.315)
0.017 (0.7)
0.14 (0.006)
0.077 (0.006)
)0.051 (<0.001)

0.979
1.007
1.057
1.099
)0.454

(<0.001)
(<0.001)
(<0.001)
(<0.001)
(<0.001)

0.263 (0.007)
0.225 (0.002)
0.34 (0.001)
0.125 (0.001)
)0.098 (<0.001)

0.724
0.388
)0.006
)0.067
)0.117

(100)
(85.33)
(34.66)
(23.33)
(3.66)

0.176
0.088
0.166
)0.059
)0.034

(0.012)
(0.055)
(0.005)
(0.026)
(0.03)

0.08 (0.207)
0.122 (0.008)
0.011 (0.719)
)0.049 (0.077)
)0.023 (0.274)

0.926 (<0.001)
1.037 (<0.001)
0.75 (<0.001)
0.025 (0.089)
)0.294 (<0.001)

0.185 (0.008)
0.382 (<0.001)
0.137 (0.018)
0.02 (0.132)
)0.102 (<0.001)

The % in Brownian motion indicates percentage of simulation was signicant. Correlograms were calculated considering two phylogenies (A and B).
Bold value signies p < 0.01

(a)

Table 3. Coecients of determination of autoregressive (ARM) and

Phylogenetic Eigenvector Regression (PVR) models for both phylogenies used in this study
Phylogeny A

Range size
Range shape
Longitude
Latitude

(b)

Fig. 2. Frequency distributions of slope (obtained from regression

among each Brownian motion simulation and phylogenetic distance
class) for phylogeny A (a) and phylogeny B (b). The arrows indicate
the slope of observed correlogram for latitude (lat), longitude (long)
range size (RS) and range shape (RSh)

have suggested that, in general, geographic range size is not

heritable (Webb and Gaston 2003, 2005; Bohning-Gaese et al.
2006; but see Jones et al. 2005 and Jablonski 2008), strongly
J Zool Syst Evol Res (2010) 48(2), 102108
 2009 Blackwell Verlag GmbH

Phylogeny B

ARM

PVR

ARM

PVR

0.080
0.035
0.890
0.109

0.204
0.104
0.953
0.272

0.056
0.043
0.870
0.169

0.203
0.099
0.912
0.293

subjected to stochastic processes (Gaston and He 2002) and

phylogenetically labile (Diniz-Filho and Torres 2002; Liow
and Stenseth 2007). Moreover, ddler crabs are costal
organisms, occupying both continental and island habitats
and the coast-lines of island and continental dier in size and
shape. Thus, the lack of phylogenetic signal in geographic
range size and shape may result from island phenomenon
(sensu Losos 2008), mainly, because the insular habitats have
a high evolutionary rate (Schluter 2000) as a consequence of
adaptive radiation, and this high evolutionary rate produced
low phylogenetic signal (Revell et al. 2008). We used 88
species in our analysis, out of which 11% occur in insular
habitat, and 30% occur in both habitats (insular and
continental). Other papers demonstrated the weak phylogenetic signal in traits of insular species (Losos and Glor 2003;
Knouft et al. 2006).
Moreover, some papers have suggested that the power to
detect phylogenetic signal is scale dependent (in terms of
spatial and taxonomic resolution). This way, phylogenetic
signal may be detected more frequently when the taxonomic
resolution of a study is expanded (e.g. all Crustaceae)
(Cavender-Bares et al. 2006). In our study, it is not possible
to test the inuence of taxonomic resolution on phylogenetic
signal, but it is important to note that other papers have tested
the heritability of geographic range size in species within the
same genus (e.g. Bohning-Gaese et al. 2006) and, in some
cases, a signicant phylogenetic pattern in geographic range
size was detected only below the tribe level (Blackburn et al.
2004). This way, the inuence of taxonomic resolution on
phylogenetic data need more test and, until present, this
relationship is not clear (Losos 2008).

Phylogenetic autocorrelation and heritability of Uca

We tested the inuence of spatial extent in our analyses by
considering two geographic realms, namely the American (with
51 species) and Indo-West species (37 species). The results of the
ARM revealed that the phylogenetic signal of geographic range
size and shape remained low in both biogeographic regions (in
Indo-West Pacic only 11% of the variation in range size and
<0.01% of the variation in range shape could be explained by
phylogeny, whereas in America these gures were equal to 1.5%
and <0.01%, respectively results for PVR are qualitatively
similar). Moreover, the geographic range position (mainly
longitude) also loose the phylogenetic signal when the analyses
were carried out per biogeographic region (in Indo-West Pacic
only 8.8% and 1.4% of the variation in longitudinal and
latitudinal midpoints across species, respectively, could be
explained by phylogeny; whereas in America these gures were
equal to 10.3% and 30.4%, respectively). Thus, within each
realm, all geographic range attributes presented weak phylogenetic signal. Probably, within realms, the relationships among
species are overdispersed (Cavender-Bares et al. 2006). Therefore, the global scale is more adequate to detect the phylogenetic
signal in geographic range properties.
Finally, our phylogenetic autocorrelation analyses suggested
that the macroecological traits analysed (geographic range
size, shape and position) do not follow a Brownian motion
process, with marked deviations (but of dierent natures)
occurring in geographic range size, shape, latitudinal and
longitudinal position. The deviations from Brownian motion
indicate that more complex adaptive processes creating evolutionary lability can explain the evolution of these traits,
instead of simple stochastic variation in the course of
phylogeny (Diniz-Filho 2001).
Recently, a debate about the role of niche conservatism in
establishing macroecological and macroevolutionary patterns
has emerged (see Wiens and Graham 2005; Losos 2008; Wiens
2008), and detecting this pattern is strongly aected by how
neutral models of evolution are incorporated into the data
analyses. The niche conservatism is the tendency of species to
preserve ancestral ecological characteristics (e.g. attributes of
geographic range). However, the phylogenetic signal and
phylogenetic niche conservatism were dierent, mainly because
the phylogenetic niche conservatism refers to the phenomenon
that closely related species are more ecologically similar than
might be expected by Brownian motion (Losos 2008). In our
study, we were able to dierentiate these two phenomena
because we compared observed patterns with those derived
from Brownian motion simulations along the phylogeny of
ddler crabs. In one hand, the absence of phylogenetic signal
indicates that phylogenetic niche conservatism does not occur
(Losos 2008). Therefore, weak phylogenetic signal found for
geographic range size and shape shows plasticity among
species and very quick responses after speciation, without
conservatism in evolutionary time in these attributes. Only the
geographic range position (longitude) of ddler crabs showed
phylogenetic patterns and related species are more similar than
expected by a pure Brownian motion (i.e. larger Morans I ).
Geographically, after the speciation the new species tend to
remain closer across longitudinal axis than expected by a pure
diusion process in space and time. Although it is dicult to
establish why this pattern appears (i.e. longitudinal physical
barriers or environmental constraints), our analysis support
niche conservatism pattern across longitudinal range expansion throughout the evolution of the genus.

107

Acknowledgements
JCN and LCT received a scholarship from CAPES. LMB and JAFDF
are supported by productivity grants from Brazilian CNPq and by
Fundacao de Amparo a` Pesquisa da Universidade Federal de Goias
(FUNAPEUFG).

Resumen
Correlogramas logeneticos y herencia de la posicion geograca, forma y
tamano de rango de cangrejo violinista, genero Uca
El objetivo de este trabajo fue estimar los niveles de herencia logenetica
existentes en la posicion geograca, forma y el tamano de rango
geograco en 88 especies de cangrejo violinista del mundo, mediante
simulaciones y metodos comparativos logeneticos para as evaluar su
ajuste al modelo neutro de evolucion browniana. Los mapas de rango
geograco se obtuvieron de la literatura. La forma de rango geograco
fue estimada en la dimension fractal. Los patrones evolutivos en el
tamano y forma del rango geograco y la posicion geograca fueron
explorados mediante correlogramas logeneticos utilizando el ndice I
de Moran, coecientes autorregresivos (ARM) y regression por
autovetores logeneticos (PVR). Estos correlogramas fueron comparados con aquellos obtenidos mediante la simulacion de procesos de
evolucion browniana en las logenias. El tamano y forma de rango
geograco del cangrejo violinista mostro una distribucion apuntada
hacia la derecha aunque no se encontro autocorrelacion logenetica.
Por otra parte, se observo un marcado patron logenetico para la
posicion geograca del rango (principalmente a lo largo del eje
longitudinal). De hecho, el ARM y PVR evidencio respectivamente
que cerca del 86% y 91% de la localizacion del punto medio
longitudinal del rango se puede explicar mediante las relaciones
logeneticas existentes entre las especies. El fuerte patron logenetico
en la longitud podr a ser debido a especiacion alopatrica y a una
cladogenesis estructurada geogracamente para el grupo, tal y como se
propuso en las hipotesis. Los rasgos analizados (rango geograco y
posicion geograca) no siguieron un proceso de evolucion browniana,
sugiriendo pues que tanto los procesos evolutivos como la adaptacion
ecologica deber an ser tenidos en cuenta para explicar sus dinamicas, ya
que el transcurso de la evolucion del cangrejo violinista no se explica
mediante un simple modelo de herencia neutra.

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