Further twists in gastropod shell evolution

Abstract

The manner in which a gastropod shell coils has long intrigued laypersons and scientists alike. In evolutionary biology, gastropod shells are among the best-studied palaeontological and neontological objects. A gastropod shell generally exhibits logarithmic spiral growth, right-handedness and coils tightly around a single axis. Atypical shell-coiling patterns (e.g. sinistroid growth, uncoiled whorls and multiple coiling axes), however, continue to be uncovered in nature. Here, we report another coiling strategy that is not only puzzling from an evolutionary perspective, but also hitherto unknown among shelled gastropods. The terrestrial gastropod Opisthostoma vermiculum sp. nov. generates a shell with: (i) four discernable coiling axes, (ii) body whorls that thrice detach and twice reattach to preceding whorls without any reference support, and (iii) detached whorls that coil around three secondary axes in addition to their primary teleoconch axis. As the coiling strategies of individuals were found to be generally consistent throughout, this species appears to possess an unorthodox but rigorously defined set of developmental instructions. Although the evolutionary origins of O. vermiculum and its shell's functional significance can be elucidated only once fossil intermediates and live individuals are found, its bewildering morphology suggests that we still lack an understanding of relationships between form and function in certain taxonomic groups.

Full text

Biol. Lett. (2008) 4, 179–182
doi:10.1098/rsbl.2007.0602
Published online 8 January 2008
Evolutionary biology
Further twists in gastropod
shell evolution
Reuben Clement s
1,
*
, Thor-Seng Liew
2
,
Jaap Jan Vermeulen
3
and Menno Schilthuizen
2,4
1
World Wide Fund for Nature-Malaysia, 49, Jalan SS23/15,
47400 Petaling Jaya, Selangor, Malaysia
2
Institute for Tropical Biology and Conservation, Universiti Malaysia
Sabah, Locked Bag 2073, 88999 Kota Kinabalu, Malaysia
3
Nationaal Herbarium Nederland, PO Box 9514, 2300 RA Leiden,
The Netherlands
4
National Museum of Natural History ‘Naturalis’, PO Box 9517,
2300 RA Leiden, The Netherlands
*Author for correspondence (clements@alumni.nus.edu.sg).
The manner in which a gastropod shell coils has
long intrigued laypersons and scientists alike. In
evolutionary biology, gastropod shells are among
the best-studied palaeontological and neontolo-
gical objects. A gastropod shell generally exhibits
logarithmic spiral growth, right-handedness and
coils tightly around a single axis. Atypi cal shell-
coiling patterns (e.g. sinist roid growth, uncoiled
whorls and multiple coiling axes), however,
continue to be uncovered in nature. Here, we
report another coiling strategy that is not only
puzzling from an evolutionary perspective, but
also hitherto unknown among shelled gastro-
pods. The terrestr ial gastropod Opisthostoma
ver miculum sp.nov.generatesashellwith:
(i) four discernable coiling axes, (ii) body whorls
that th rice detach and twice reattach to preced-
ing whorls without any reference support, and
(iii) detached whorls that coil around three
secondaryaxesinadditiontotheirprimary
teleoconch axis. As the co iling strateg ies of
individuals were found to be generally consistent
throughout, this species appears to possess an
unorthodox but rigorously defined set of develop-
mental instructions. Although the evolutionary
origins of O. vermiculum and its shell’s functional
significance can be elucidated only once fossil
intermediates and live individuals are found, its
bewildering morphology suggests that we still lack
an understanding of relationships between form
and function in certain taxonomic groups.
Keywords: conchology; snail; karst; Malaysia;
Mollusca; morphology
1. INTRODUCTION
Over the past 150 years, evolutionary biology has
benefited from the many qualities of the gastropod shell
(Schilthuizen 2002). It is essentially a complex three-
dimensional structure that acts as the snail’s interface
with the biotic and abiotic environments. Conse-
quently, it is of great importance for survival and the
target of multifarious natural (and possibly sexual;
Schilthuizen 2003) selection pressures. Yet, it answers
to a very limited set of growth parameters, which makes
its evolution reducible to few character-state changes
(Thompson 1942). The gastropod evolutionary history
reveals a dominance of shells resembling helicospiral
cones that monotonically expand according to a logar-
ithmic function ( Thompson 1942 and references
therein). In addition, most shells are right handed and
possess overlapping whorls that coil around a single axis
(figure 1a). Spiral coiling also appears to be dictated by
a set of ‘behavioural’ rules involving shell sculpture. For
example, Hutchinson’s (1989) road-holding model
(RHM) postulates that shell ornamentation (e.g. keels
and low curvature areas) is the vital reference spot for
the attachment of subsequent whorls.
Several groups of gastropods, however, possess
shell-coiling patterns that depart from the above-
mentioned conventions. For instance, shells of
marine vermetids generally deviate from logarithmic
spiral growth late in their ontogeny. In the terrestrial
genus Opisthostoma, shells are not right handed, but
‘sinistroid’ (figure 1c) due to a reversal in coiling
direction in the last half-whorl (Gittenberger 1995).
Furthermore, Opisthostoma shells can possess two
(e.g. Opisthostoma concinnum ; figure 1b)orthree
different coiling axes (e.g. Opisthostoma castor). In
another terrestrial genus, Ditropopsis, the body whorls
can detach to produce an ‘uncoiled’ shell (figure 1d ).
Interestingly, detached whorls of uncoiled gastropods
do not adhere to the sculptural features of previous
whorls; they remain either coiled around the primary
teleoconch axis (figure 1d ) or coil in an irregular
manner (e.g. marine vermetids).
Taking these exceptions into account, we can refine
our earlier generalizations of gastropod shells: (i) they
possess an upper limit of three coiling axes, (ii) detached
body whorls do not reattach to the preceding whorls,
and (iii) whorls once detached either coil around a
primary teleoconch axis or deviate haphazardly. In this
paper, we describe a new species of terrestrial gastropod
with a shell that pushes these evolutionary boundaries
even further. In addition, we discuss its evolutionary
origins, functional significance and coiling strategy.
2. MATERIAL AND METHODS
The specimens upon which the species description was based were
deposited in the Zoological Reference Collection (ZRC), Mollusc
Section (MOL), Raffles Museum of Biodiversity Research ( RMBR)
and National University of Singapore. Using visual inspection and
flotation techniques to extract shells, 38 individuals (including fresh
dead specimens) were obtained from a total of six different 8 m
2
plots at the type locality. Descriptions are based on the shell
characters and nomenclature follows van Benthem-Jutting (1952)
and Vermeulen (1994). Measurements of shells were based on
images obtained from a scanning electron microscope and are in
millimetre. Height refers to the longest dimension of the shell,
while width refers to its perpendicular dimension.
3. SYSTEMATICS
Higher taxon names: Mesogastropoda Thiele 1925;
Diplommatinidae Pfeiffer 1856; and Genus Opisthos-
toma Blanford & Blanford 1860.
(a) Type species
Opisthostoma nilgiricum Blanford & Blanford 1860.
(b) Description
(i) Opisthostoma vermiculum Clements & Vermeulen,
n. sp.
Height:holotype1.5,paratype1.5.Width:holotype0.9,
paratype 1.0. Shell thin, cream or white, not transparent
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2007.0602 or via http://journals.royalsociety.org.
Received 1 December 2007
Accepted 7 December 2007
179 This journal is q 2008 The Royal Society

and slightly shiny. First whorl smooth; subsequent
whorls sculptured with fine, white, regularly spaced
radial ribs, becoming widely spaced and flared
nearing aperture before being compressed; spiral striae
absent. Whorls 4.5–5, convex, increasing in radius,
uncoiling at the end of second whorl; detached third
whorl returns to reattach to the base of second whorl,
followed by a phase of detachment, reattachment and
detachment; whorls deviate from primary teleoconch
axis to coil around three additional axes. Suture deep.
No umbilicus. Aperture round, vertical, without
teeth. Peristome duplex, continuous, circular to
rounded triangular.
(c) Remarks
An internal constriction, which qualifies placement
under the genus Opisthostoma (see Vermeulen 1994),
was detected in this species. All 38 specimens demon-
strated four changes in the coiling direction and
underwent similar detachment–reattachment phases,
but displayed slight variations in the angles of each
coiling axis (see electronic supplementary material).
Intraspecific variation (nZ6) among shell dimensions
appeared to be low, with a mean (Gs.d.) height and
width of 1.5G 0.1 and 0.9G0.1, respectively.
(d) Types, locality and distribution
Holotype: ZRC.MOL.002824, Gunung Rapat
(48 33
0
N, 1018 7
0
E), Perak, Peninsular Malaysia,
held in RMBR. Two paratypes: ZRC.MOL.002825
and ZRC.MOL.002826, same data as holotype.
Known only from the type locality.
(e) Etymology
‘vermiculum’ meaning wormy, as the shell resembles a
worm-like organism. Clements and Vermeulen are
assigned as authors for O. vermiculum sp. nov.
4. DISCUSSION
Evolutionary responses of shell traits to environmental
pressures are among the best-documented microevolu-
tionary processes (Endler 1986). For example, uncoil-
ing in freshwater gastropods appeared to correspond
with periods of high chemical stress during the
Miocene epoch ( Nutzel & Bandel 1993). The impact
of environmentally induced mutations (figure 1e)on
the phenotype of O . vermiculum, however, cannot be
ascertained without fossil records and historical
environmental data. Novel shell characters can also
result from hybridization (Woodruff & Gould 1987),
during which the developmental factors or the gene
(a)
(b)
(c)
(d )
(e)
Figure 1. Different gastropod shell-coiling patterns. (a) Queridomus conulus exhibiting logarithmic helicospiral growth with
tightly coiled whorls around a single axis (black line), (b) O. concinnum and (c) Opisthostoma hailei exhibiting ‘sinistroid’
growth with two different coiling axes (black lines), (d ) Ditropopsis sp. demonstrating uncoiling with detached whorls that
never reattach and (e) a mutant individual of O. hailei. Scale bars, 200 mm.
180 R. Clements et al. Further twists in gastropod shell evolution
Biol. Lett. (2008)

interactions related to morphologies of different species
produce new features (Chiba 2005). However, the
distinctive and invariant coiling patterns of O. vermiculum
specimens examined in our study suggest that its
conchology is under fairly strict developmental–genetic
control and is unlikely to be a product of hybridization
between two other congeners that occur sympatrically on
thesamekarst—Opisthostoma megalomphalum and
Opisthostoma paulucciae; obvious differences in their shell
sculpture (e.g. rib spacing and presence of apertural
flares) further reduce the likelihood that O. vermiculum is
an intermediate species.
The gastropod shell sculpture could have evolved
to cope with predation (Palmer 1977), feeding (Illert
1981) or movement (Cain & Cowie 1978). In some
species of Opisthostoma, the evolution of intricate shell
ornamentation may be driven by sexual selection
(Schilthuizen 2003), although empirical evidence thus
far suggests only the role of ‘Red Queen’ coevolu-
tionary interactions with the snails’ predators
(Schilthuizen et al. 2006). The functional significance
of uncoiling (especially in O. vermiculum), however,
remains unclear ( Morton 1965; Nutzel & Bandel
1993). Uncoiled shells may facilitate predator evasion
in some species (i.e. whorl detachment makes snails
effectively larger; Rex & Boss 1976), but appear
energetically disadvantageous to construct (i.e. uncoil-
ing weakens shells and consumes additional shell
material; Rex & Boss 1976) and may even hinder
movement (Clarke 1973). Uncoiling has also been
associated with sessility (e.g. in marine gastropods;
Gould 1968) and gerontic conditions ( Yo c h e l s o n
1971), but the former is precluded in terrestrial snails
and the latter is unlikely because whorl detachment in
O. vermiculum begins early in its ontogeny.
The coiling axis of a gastropod shell is not easily
discernable (Okamoto 1988; Savazzi 1990), but
numerous ‘fixed axes’ mathematical models have
been used to explain shell geometries (Raup 1961;
Raup & Michelson 1965; Løvtrup & Løvtrup 1988;
Illert 1989; Savazzi 1990).Thepresenceoffour
coiling axes in O. vermiculum (figure 2b), which is the
highest number known for a shelled gastropod, poses
a challenge to the development of a model that
accounts for such a morphologically bizarre shell.
Reorientation of shell-coiling axes has been attributed
to a simple rotation of the snail body inside the shell
(Ackerly 1989). A more remarkable and unique
aspect, however, is the departure of the second whorl
from the primary teleoconch axis to revolve around a
secondary (almost perpendicular) axis before latching
back onto the preceding whorl (figure 2c), after
which it proceeds to a detachment–reattachment
(figure 2d )–detachment phase. The importance
of shell ornamentation (e.g. keels and ribs) for
spiral coiling has been corroborated by experimental
(a)
(b)
(c)
(d )
Figure 2. Opisthostoma vermiculum sp. nov. (a) Ventral view, (b) side view indicating four coiling axes (white lines), (c)first
and (d ) second reattachment points of detached whorls (white arrows). Scale bar, 100 mm.
Further twists in gastropod shell evolution R. Clements et al. 181
Biol. Lett. (2008)

tests on the RHM (e.g. Checa et al. 1998), but the
detached whorls in O. vermiculum consistently reat-
tach to preceding whorls without any apparent need
for reference support.
Ultimately, the functional significance and coiling
regulatory mechanism of the shell in O. vermiculum
cannot be investigated without studying live individuals,
but the novelty of its shell-coiling pattern is indisputable.
It is also interesting to note that such phenotypic
peculiarities often occur among microgastropods (less
than 5 mm) such as Opisthostoma. Unfortunately,
Opisthostoma snails are particularly vulnerable to extinc-
tion (IUCN 2004) as most species are restricted to
limestone karsts (Vermeulen 1994), which have become
increasingly threatened by quarrying activities
(Clements et al. 2006). We hope the finding of this
species will not only encourage further research into the
relationship between form and function in gastropods,
but also promote more inventories of limestone karsts
due to their potential for yielding important taxonomic
and evolutionary discoveries (e.g. Morwood et al. 2004).
This project was supported by a research permit (no. 1773,
Economic Planning Unit, Malaysia) and grants from the
Singapore Zoological Gardens and the National University
of Singapore (R-154-000-264-112). We are grateful to
David Bickford, Lahiru Wijedasa, Matthew Lim, Nalini
Puniamoorthy and Stephen Ambu for their comments and
assistance. We also thank two anonymous referees and
Geerat J. Vermeij for greatly improving the manuscript.
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