MORPHOLOGICAL DIVERGENCE AS A RESULT OF COMMON
ADAPTATION TO A SHARED ENVIRONMENT IN LAND SNAILS
OF THE GENUS HIRASEA
SATOSHI CHIBA
Department of Ecology and Evolutionary Biology, Graduate School of Life Sciences, Tohoku University, Aobayama, Sendai 980-8578, Japan
(Received 30 October 2008; accepted 2 March 2009)
ABSTRACT
Mechanisms constraining phenotypic evolution, such as functional trade-offs, can cause phenotypic
divergence in a common adaptation to use of the same habitat. This hypothesis was tested by field
observations and laboratory experiments in Hirasea, a genus of endemic land snails of the Ogasawara
Islands. Hirasea operculina was found on the large leaves of palm trees and possessed an extremely flat
shell. In some localities, H. chichijimana and H. diplomphalus tended to rest on the leaves of broadleaved trees and on palm leaves, respectively, and in these localities these species possess a flat shell
relatively similar to each other, although the former has a smaller number of whorls and a higher
spire than the latter. In other localities, both of these species were found inside deep soil and with no
difference in habitat use. In these cases, both species have a higher shell, but their morphologies are
very different: H. chichijimana possesses a conical shell with a high spire and a small aperture, but
H. diplomphalus has a discoidal shell with a deeply sunken spire and a large aperture. Experiments
measuring the time needed for the snail to escape from a light to hide under artificial substrates
showed that flatter shells were more advantageous to movement on substrates with foliated structures
such as leaf litter, while higher shells were more advantageous on substrates with a fine particle structure such as soil. In one case, a relatively higher shell has been attained by a decrease of whorl
expansion rate and an increase of whorl translation rate along the coiling axis (resulting in a highconical shell with a high spire), and in the other by an increase of whorl expansion rate and a
decrease of whorl translation rate (resulting in a discoidal shell with a sunken spire). Both appear to
be adaptive responses to the same burrowing lifestyle. These findings suggest that phenotypic traits
can be diverse, even if they result from a common adaptation to a shared environment, if the
adaptive changes have occurred from different starting points.
INTRODUCTION
In models of the relationship between niche and phenotype,
the resource (habitat) and phenotype axes are assumed to map
one-to-one (Taper & Case, 1985) and phenotypic traits are
assumed to correlate with similarity in habitat use (Schluter,
2000). Nevertheless, these assumptions can be hard to verify.
Although correlations between optimal resource types and phenotypes have been reported in some studies, such a relationship
is often obscure (Futuyma & Moreno, 1988). In particular,
functional trade-offs in resource-handling strategies may result
in different optimal phenotypes for use of the same resource
(Smith, 1987; Adams and Rohlf, 2000; DeWitt et al., 2000;
Svanbäck & Eklöv, 2003; Konuma & Chiba, 2007). The possible existence of different strategies to serve the same function,
or of adaptive changes to use the same resource or habitat,
may cause divergence of phenotypes. A number of studies have
shown that parallel evolution has occurred in two or more
lineages that have made the same adaptive shift, producing
similar morphologies (Schluter, 2000). This suggests that the
adaptive changes should take the shortest route to the same
end. Furthermore, if the adaptive changes have occurred from
rather different starting points, common adaptation may result
in different morphologies.
In testing this hypothesis, land snails are useful because of
their diversity in ecology and morphology and constraints in
variation of shell traits (Gould, 1984, 1989; but see criticisms
Correspondence: S. Chiba; e-mail: [email protected]
by Stone, 1996). Land snails have made a significant contribution to our understanding of how morphological variability
is created through selection by ecological and environmental
factors (Davison, 2002). Shell morphology is often associated
with particular habitat characteristics (Cain, 1978, 1983;
Goodfriend, 1986; Heller, 1987; Cameron & Cook, 1989; Cook,
1997; Chiba, 1999, 2004; Chiba & Davison, 2007). For
example, species that forage on horizontal substrates tend to be
low-spired (Cain, 1978, 1983), because relative spire height
correlates with the inclination of the surface on which the
snails live, which may be related to the mechanics of carrying
a shell of particular shape (Cain & Cowie, 1978; Cameron &
Cook, 1989; Cowie, 1995).
In the present study, the hypotheses of close association
between shell shape and habitat use, and of divergence in morphological traits resulting from a common adaptation to a
shared environment, are tested by field observations and laboratory experiments on endemic land snails, genus Hirasea
(Euconulidae), of the Ogasawara Islands in the western
Pacific. Hirasea provides an excellent model system to address
the above issues, because it has undergone extensive adaptive
radiation within the Ogasawara Islands. Although species of
Hirasea are tiny (3–6 mm diameter), they show unusual morphological diversity, not only among species but also within
species, including extremely flat, lens-like shells, high conical
shells and discoidal shells with a deeply sunken spire (Fig. 1).
It is expected that their morphological diversity should be
closely associated with differences in habitat use (leaf-litter
layer or soil) and lifestyles among populations; however, very
Journal of Molluscan Studies (2009) 75: 253–259. Advance Access Publication: 6 May 2009
# The Author 2009. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved.
doi:10.1093/mollus/eyp020
S. CHIBA
Figure 1. Diversity and geographical variation in shell morphology of Hirasea in Anijima. A, B. Hirasea chichijimana. C, D. H. diplomphalus.
E, F. H. operculina.
little is known about the ecology of Hirasea or what drives
diversity in this unique group. These expectations are tested in
Hirasea by examining habitat use and morphological variation
and by experiments comparing the performance of different
shell shapes in habitat with different spatial structure created
with artificial substrates.
MATERIALS AND METHODS
Sampling, habitat scoring and data analysis
Sampling and habitat analysis were carried out at 25 study
sites on Anijima Island in the Ogasawara Islands (Fig. 2,
Supplementary material, Appendix A) with three species of
Hirasea: H. operculina (Gould, 1859), H. chichijimana Pilsbry,
1902 and H. diplomphalus Pilsbry, 1902. These study sites were
selected because habitat condition (vegetation, moisture, pH)
was similar to each other (Chiba, 2007). Anijima is a fairly
uniform island both geologically and topographically and is
approximately 8 km2 in area. The structure of the forest and
the forest floor environment is very simple; the forest floor is
open with no bush or grass ground cover. The litter layer is
composed mainly of palm and pandanus leaves, small
branches, and the leaves of broad-leaved trees such as Distylio
lepidotum and Pouterietum dubiae (Chiba, 2007). Palm leaves are
hard and large with an area of approximately 0.2– 0.5 m2.
Pandanus leaves are also hard and fairly large with an area of
0.02 –0.1 m2. The leaves of the broad-leaved trees are small,
,0.005 m2 in area. The soil layer under the leaf litter was dry
and aggregated, and is formed of hard and large (2 –5 mm in
diameter) lumps of soil rather than being sandy.
A 10 m 10 m quadrat was placed at each study site, and
snails were searched for in the litter and the soil under the
litter within the quadrat. The quadrat was first divided into
one hundred 1 1 m squares. Each 1 1 m square was
Figure 2. Maps of the Ogasawara Islands and Anijima with locations
of the study sites.
254
MORPHOLOGICAL DIVERGENCE IN LAND SNAILS
divided into four 0.25 m2 sites, making 400 squares in total for
each study site. Numbers from 1 to 400 were assigned to each
of these squares, and 40 squares were selected using a random
table. Snails living on the ground were collected from forty
0.25 m2 frames placed on the floor of the randomly selected
squares. All leaves in the litter within the frame were carefully
removed and snails were searched for on both leaves and soil.
When a live snail was found, the position in the litter and the
type of substrate on which it sat was scored. The vertical position of the snail was recorded in three categories: ‘upper litter
layer’, ‘lower litter layer’ and ‘inside the soil’. The position of
snails on the soil/litter junction was scored as ‘lower litter
layer’“. Because the distinction between the upper and lower
parts of the litter is vague, ‘upper litter layer’ here designates
the uppermost leaves, and ‘lower litter’ the remaining parts of
the litter. The substrate was recorded as ‘palm leaves’, ‘pandanus leaves’, ‘leaves of broad-leaved trees’, and ‘soil’. Decayed
wood was recorded as ‘soil’. Fallen tree branches were recorded
as ‘leaves of broad-leaved trees’ because all these branches and
twigs were small and from broad-leaved trees.
After the species were recorded, all snails except those to be
used for laboratory experiments were returned to the quadrat
from which they were collected. Because all Hirasea species are
endangered, empty shells were collected from the same
quadrat and taken to the laboratory for shell measurements to
minimize damage to the populations. The populations were
subsequently monitored.
The proportion of each microhabitat used by the snails was
calculated for each species at each quadrat. The simplified
Morisita’s index (Horn, 1966) was used to calculate the pairwise similarity of microhabitat use between populations. The
greater the similarity between population pairs, the more ecologically similar they are. Similarities in habitat use among
populations were visualized with multidimensional scaling
(MDS), a robust ordination technique. An MDS was applied
to the matrix of the Morisita’s index. All the stress values
obtained were sufficiently low, indicating the excellent fit of
the two-dimensional solution. Consequently, habitat use of
populations was analysed by using the two-dimensional MDS
plot. Associations between litter depth and coordinate values
obtained by MDS were examined using regression analyses.
Figure 3. A, B. Measurements of the shells of Hirasea used in the
morphological analysis: shell diameter (D), shell height (H), apertural
width (AW), apertural height (AH), height of spire (SH), number of
whorls (N). SH of shells with a sunken spire (B) was calculated as
E/tan u.
the percent of the total variance explained by the factor was
,10%, the factor was dropped from the analysis. The PCAs
were done in SYSTAT 10 (SPSS, 2000).
Laboratory experiments
Snail locomotive performance was quantified on different substrates to test the hypothesis that shell-shape variation affects
fitness in habitats with different spatial structure. To simplify
and idealize the spatial structure of the habitat, two types of
artificial substrate were used in the experiments: piles of filter
papers and masses of small glass beads, which imitated the
litter layer and aggregated soil, respectively. Filter paper
(Advantec no.1, 0.2 mm thickness) was cut into 3 cm 3 cm
squares and placed horizontally in each of 10 containers
(100 150 mm) to a depth of 30 mm. In each of the other 10
containers, glass beads (fine no. 3, 3 mm diameter) were
placed to a depth of 30 mm.
Twenty live snails of each species were collected and used for
the experiment. First, each snail was activated by wetting it,
then placed on the filter paper or glass beads in the container
and exposed to light emitted by a halogen lamp (PLH-150,
NPI, 180,000 LX) at a distance of 25 cm. Because Hirasea exhibits strong negative phototaxis, snails should immediately start
to move to the underside of the substrates. Before snails were
placed on the substrates, water was sprayed on the substrates five
times for each treatment. The escaping snails should either hide
in the space between the pieces of filter paper or burrow into the
mass of glass beads. The time between the snail starting to crawl
and complete disappearance of its shell under the paper or glass
beads was measured. The time should be shorter for snails with
greater locomotive ability in the substrates. Each treatment was
repeated 10 times for each snail. If the snail became inactive,
took more than 20 min, or reached the container wall before it
hid under the substrate, this treatment was not used in the
MORPHOLOGICAL ANALYSIS
Six measurements of the adult shells (N, number of whorls; D,
shell diameter; H, shell height; AH, aperture height; AW, aperture width; SH, spire height; Fig. 3) were made with an ocular
micrometer in a stereomicroscope. Adult snails were defined as
having a shell with a strongly thickened outer lip. For snails
with sunken spires, the spire height was given a negative value
and calculated as the spire radius multiplied by the tangent of
the angle between the coiling axis and the descending whorl
profile (Fig. 3). The angle was measured by tilting the stage on
which the snail was placed. Because the angle was difficult to
measure at the aperture of a sunken-spired shell, the spire
height was calculated from measurements taken half a whorl
back from the aperture.
Relationships among the morphological variables were
examined by principal component analysis (PCA, R mode) on
the correlation matrix. PCA was used on the correlation
matrix because one of the variables (number of whorls) did
not have the same dimension, and because a PCA on a correlation matrix applied to transformed data is equivalent to a
variance-covariance matrix analysis. Eigenvectors were rotated
using varimax rotation and retained when the explained variance was higher than that of unrotated components or when
the interpretation of PCs was easier. Data were logtransformed to remove possible allometric influences. When
255
S. CHIBA
analyses. Shell characters were measured for each snail and
associations between shell characters and the time to become
hidden were examined by a generalized linear mixed model
(GLMM) using maximum likelihood in R 2.6.1 (R
Development Core Team, 2006) and the ‘nlme’ library
(Pinheiro & Bates, 2000).
use of H. chichijimana from locations 3 and 12 fell within the
range of populations of H. diplomphalus, which had the lowest
scores on both coordinates 1 and 2 (Fig. 4). These populations
of H. chichijimana had the greatest preference for sitting in the
soil, similar to H. diplomphalus.
Morphological variations
RESULTS
Together, the first three principal components explained more
than 90% of the variance in all three species (Table 1). The
PC2 scores indicated shell size for all species. Loading of
H. diplomphalus PC1 showed that relative shell height (H) was
positively correlated with aperture height (AH), and negatively
correlated with the number of whorls (N) and spire height
(SH) (Table 1). In contrast, loading of PC1 of H. chichijimana
and H. operculina showed that H/D was positively correlated
with N and SH (Table 1). These results show that when the
shells of H. chichijimana and H. operculina become higher, the
spire of these species become more pronounced and
the number of whorls increases. When its shell is flatter,
H. diplomphalus has a barely protruding spire (Fig. 5).
However, as the shell of H. diplomphalus becomes relatively
higher, its spire becomes concave, the aperture becomes larger
and the number of whorls decreases. As a result, the relatively
highest shell of this species possesses a shell with a deeply
sunken spire (Fig. 5), large aperture, and a small number of
whorls.
When their shells were flattest, the shell outlines of
H. chichijimana and H. diplomphalus were fairly similar to each
other (Fig. 5), whereas the number of whorls of these species
was different. In addition, the spire was slightly higher in
M. chichijimana than in M. diplomphalus. When their shells
were taller, the number of whorls of H. chichijimana and
H. diplomphalus was similar to each other. The shell of
H. operculina was much flatter than those of the other two
species, because H. operculina had a shell with a much flatter
aperture.
Population habitat use was compared with relative shell
height (H/D) as a representative of the variations in PC1
scores. Significant negative correlations between MDS coordinate 1 and mean H/D were found in H. chichijimana
(R ¼ 20.884, P , 0.0001) and H. diplomphalus (R ¼ 20.896,
P , 0.0001), but no significant correlation was found in
H. operculina (R ¼ 0.088, P ¼ 0.686). A significant negative correlation was found between MDS coordinate 2 and mean H/D
in H. chichijimana (R ¼ 20.586, P ¼ 0.0106) and H. operculina
(R ¼ 20.463, P ¼ 0.0198), but not in H. diplomphalus
(R ¼ 20.361, P ¼ 0.155).
Habitat use
The three species of Hirasea showed differences in their preference for substrate types and positions in the litter, not only
among the different species but also among populations within
the same species (Fig. 4, Supplementary material, Appendix B).
A significant negative correlation was found between scores on
the MDS coordinate 1 and the frequency of snails sitting within
the soil (R ¼ 20.862, P , 0.0001), and a significant positive
correlation between scores on the MDS coordinate 1 and
frequency of snails resting in the upper litter layer (R ¼ 0.986,
P , 0.0001). Accordingly, lower scores on this coordinate were
interpreted as a greater preference for the deeper part of the
litter. A significant positive correlation was found between
scores on the MDS coordinate 2 and the frequency of snails
resting on the leaves of broad-leaved trees (R ¼ 0.906, P ,
0.0001). Therefore, higher scores on this coordinate were interpreted as greater preference for the leaves of broad-leaved trees.
Hirasea operculina showed the highest scores on coordinate 1
and low scores on coordinate 2. This suggests that H. operculina
prefers to sit on palm leaves in the upper litter layer. Most
populations of H. diplomphalus showed the lowest scores on coordinate 1 and therefore these populations prefer to sit inside the
soil. However, populations of H. diplomphalus in locations 6, 17
and 18 showed high scores on coordinate 1, which implies that
they were not in the soil, but at a similar depth in the litter as
H. chichijimana despite differences in their scores on coordinate
2. Most populations of H. chichijimana showed medium scores
on coordinate 1 and high scores on coordinate 2. This implies
that these populations of H. chichijimana prefer to sit on the
leaves of broad-leaf trees in the litter layer. However, habitat
Table 1. Results of principal components factor analysis for Hirasea
diplomphalus, H. chichijimana and H. operculina. Factor loadings and
percent of total variance explained by each factor are shown for each
species.
D
H
H. chichijimana
H. operculina
PC1
PC1
PC1
PC2
0.296
20.94
PC2
20.169
0.972
20.314
20.945
0.298
0.984
0.041
0.945
0.265
0.909
20.377
0.912
0.316
0.958
20.359
20.926
0.946
0.262
AW
0.025
0.98
N
20.89
0.923
PC2
0.942
SH
AH
Figure 4. Scatter plots between scores on the MDS coordinate 1 and
coordinate 2. Closed circles, H. chichijimana; open circles,
H. diplomphalus; open squares, H. operculina. Number of each plot
indicates locality of each population (see Supplementary material
Appendix A for localities).
H. diplomphalus
20.2
20.35
0.303
0.435
20.417
0.661
0.545
0.811
20.413
0.798
0.405
Percent of total variance explained
58.35
256
37.01
45.17
39.17
50.42
39.69
MORPHOLOGICAL DIVERGENCE IN LAND SNAILS
is a result of adaptation to divergent habitat use among
populations. It is suggested that the higher shell is advantageous for a burrowing lifestyle and for living in substrates
with fine particle structure. This is because the shell is higher
in populations living in broad-leaf litter than in palm-leaf litter
and is highest in populations living in the soil. In contrast, the
extremely flat, lens-like shell of H. operculina represents an
adaptation for living on the large and flat leaves of palm
or pandanus. These interpretations are corroborated by
laboratory experiments demonstrating that snails with flatter
shells hid more quickly between thin pieces of paper than did
snails with taller shells, while snails with higher shells burrowed into the mass of small glass beads more quickly than did
snails with flatter shells. Hence, a flatter shell permits greater
locomotive performance in foliage habitats (e.g. palm-leaf
litter), while a higher shell permits better performance in
habitats with fine particle structure (e.g. aggregated soil). This
probably affects snail fitness through advantages in predator
evasion or from avoidance of overheating by exposure to
sunlight.
Although the association between habitat use and relative shell
height is consistent among species, the associations between
habitat use and other shell variables (spire height, aperture
width, number of whorls) differ among species. Where
H. chichijimana and H. diplomphalus live in the upper parts of
broad-leaf litter and palm-leaf litter, respectively, both of them
possess similarly flat shells with low convex spires. However,
when these two species live in the soil, H. chichijimana possesses a
high conical shell with a high spire, small aperture and a large
number of whorls, while H. diplomphalus possesses a high shell
with a deeply sunken spire, large aperture and a small number
of whorls. Thus, while the habitat use of H. chichijimana and
H. diplomphalus is similar, divergences in these shell characters
occur between them.
Results of the PCA suggest that correlations among characters indicate difference in the routes taken to achieve a higher
shell between these species. These correlations reflect the
coiling geometry of the snail shell (Raup, 1966). On the basis
of Raup’s (1966) model, a relatively high shell can be attained
by two alternative processes: increase in the whorl translation
rate along the coiling axis and decrease in the whorl expansion
rate, or decrease in the whorl translation rate and increase in
the whorl expansion rate. The former process yields a shell
with a high spire, small aperture and a large number of
whorls, while the latter process produces a shell with a sunken
spire, large aperture and a small number of whorls. In Hirasea,
therefore, a sunken spire has no particular function or
ecological meaning, but is a byproduct of constructing a
high shell. Thus, the divergence of these characters between
H. chichijimana and H. diplomphalus could be argued to be a
byproduct of adaptation to the same burrowing habitat.
As an alternative hypothesis, adaptation against predator
attack may result in morphological divergence. Co-evolution
between snails and their predators, e.g. crabs (Vermeij, 1976;
West, Cohen & Baron, 1991; Marko, 2005), fish (Palmer, 1979;
DeWitt et al., 2000; DeWitt & Langerhans, 2003), birds
(Smith & Temple, 1982), lizards (Gans & De Vree, 1986),
slugs (Schilthuizen et al., 2006) and insects (Inoda et al., 2003),
has been an important mechanism generating phenotypic
diversity of snails and their predators. The presence of adaptive
trade-offs in snail shell morphology to protect against predator
attack may result in divergences in shell morphology (DeWitt
et al., 2000; Konuma & Chiba, 2007). However, the only
known native predators of small land snails in Ogasawara are
a spider (Ohyama, 1940) and a carabid beetle (Karube, 2004).
The densities of these predators are very low and their impacts
on Hirasea do not seem to be high. Although further research is
needed to evaluate the impact of native predators, adaptation
Figure 5. Scatter plots of relative shell height (H/D) vs spire height
relative to shell height (SH/H) (A) and relative shell height (H/D) vs
number of whorls (N) (B). Closed circles, H. chichijimana; open circles,
H. diplomphalus; open squares, H. operculina. Larger symbols indicate
population means; smaller symbols are for individual shells.
Locomotive performance in artificial substrates
The crawling time until the snails hid under paper was significantly positively correlated with relative shell height (H/D) in
H. chichijimana (df ¼ 18, F ¼ 9.417, P ¼ 0.0007), H. diplomphalus
(df ¼ 18, F ¼ 4.769, P ¼ 0.0425) and H. operculina (df ¼ 18,
F ¼ 5.633, P ¼ 0.029). In contrast, when glass beads were
used as substrates, the crawling time until the snails hid
under the beads was significantly negatively correlated with
H/D in H. chichijimana (df ¼ 18, F ¼ 5.053, P ¼ 0.0373) and
H. diplomphalus (df ¼ 18, F ¼ 7.156, P ¼ 0.0155), but there was
no correlation in H. operculina (df ¼ 18, F ¼ 2.984, P ¼ 0.101).
DISCUSSION
The close association between variations in shell morphology
and habitat use suggests that morphological diversity in Hirasea
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against predator attack is probably not a major factor in the
divergence of shell morphology in Hirasea.
A flat shell is the commonest form in the known species of
Hirasea. Burrowing deeply in soil is not a trait known in other
species or populations of Hirasea, and is rare in Euconulidae as
a whole. Thus, it is more likely that shells with a high spire
and shells with a sunken spire have both evolved from shells
with a low convex spire. Accordingly, adaptation to a similar
environment does not necessarily result in evolution of similar
phenotypes. The morphological traits of two species can be
divergent even though their habitat use is similar, and
adaptation towards the same niche along an environmental
gradient can result in phenotypic divergence.
The flat-shelled H. chichijimana possesses a slightly higher
spire and smaller number of whorls (larger whorl expansion
rate) than the flat-shelled H. diplomphalus. This suggests that
the former achieves a high shell more easily by increase in the
whorl translation rate and decrease in the whorl expansion rate
than by the alternative process. A more detailed analysis of the
specifics of shell shape will be made in future studies of
multiple species groups, but meanwhile these findings suggest
that the routes taken to achieve the same adaptation may be
different among the species if the starting points of the adaptive changes are different. Differences in the routes to the same
adaptive end can result in divergence of phenotypes, because
there are alternative strategies by which to achieve the same
function. The differences in the starting points and possibility
of many different but equally adaptive phenotypes may be
important in the adaptive diversification of phenotypes.
SUPPLEMENTARY MATERIAL
Supplementary material is available at Journal of Molluscan
Studies online.
ACKNOWLEDGMENTS
I thank H. Mori, D. Miura, K. Kimura, N. Tomioka, Japan
Wildlife Research Center and Ogasawara Branch Office of the
Tokyo Metropolitan Government for assistance in the field
survey. This study was conducted under permit from the
Agency for Cultural Affairs and by the South Kanto branch,
Ministry of the Environment, and was supported by grants
from the Japanese Society for the Promotion of Science and
Global Environmental Research Fund (F051).
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