Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 20052005
854
513542
Original Article
ANATOMY OF
TYLOMELANIA
T. VON RINTELEN and M. GLAUBRECHT
Biological Journal of the Linnean Society, 2005, 85, 513–542. With 14 figures
Anatomy of an adaptive radiation: a unique reproductive
strategy in the endemic freshwater gastropod
Tylomelania (Cerithioidea: Pachychilidae) on Sulawesi,
Indonesia and its biogeographical implications
THOMAS VON RINTELEN* and MATTHIAS GLAUBRECHT
Institute of Systematic Zoology, Museum of Natural History, Invalidenstr. 43, 10115 Berlin, Germany
Received 27 January 2004; accepted for publication 15 October 2004
The patterns of adaptive radiations in ancient lakes provide valuable clues to mechanisms of speciation and adaptation. In contrast to vertebrate radiations, for instance in fishes or finches, invertebrate species flocks have been
largely neglected. While the increase in molecular data narrows this gap, the anatomical basis for interpreting these
data against the background of evolutionary hypotheses is still widely lacking. Here we evaluate anatomical findings
in the live-bearing pachychilid freshwater gastropod Tylomelania, which has radiated extensively in ancient lakes
in the Indonesian island, Sulawesi; we have aimed at reconciling these data with recently obtained molecular phylogenetic evidence. Discovered more than a century ago, the speciose and phenotypically diverse species flock with
34 currently described taxa was only occasionally cited as an example of adaptive radiation in ancient lakes, while
anatomical data were entirely lacking. Our study of anatomical characters reveals very low qualitative variation at
the species level. Thus, contrary to earlier views we suggest the existence of a single monophyletic lineage endemic
to this island. The most conspicuous feature of Tylomelania is its uterine brooding strategy, i.e. retaining eggs and
embryos in the pallial oviduct. This is unique among South-East Asian pachychilids. Within the uterine brood pouch
the offspring is surrounded by considerable amounts of nutritive material produced by a very large albumin gland,
and the embryos are produced continuously. The shelled juveniles of some species are the largest known so far in
viviparous gastropods, measuring almost 2 cm in length when hatching. This combination of reproductive features
in Tylomelania, characterized by a high amount of maternal investment, is considered to be ovoviviparous, rendering
its brooding strategy unique also among other gastropods. In addition, our data reject a previously assumed close
relationship to other South-East Asian pachychilids and instead suggest the North Australian Pseudopotamis as sister group to Tylomelania. These findings have significant consequences for the phylogenetic interpretation of morphological characters of Tylomelania in an evolutionary and biogeographical context, leading to the hypothesis that
the common ancestor of both genera originated somewhere on the northern Australian continental margin. © 2005
The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542.
ADDITIONAL KEYWORDS: molecular phylogeny – reproduction - species flock - systematics - viviparity zoogeography.
INTRODUCTION
Adaptive radiations on islands represent fascinating
model systems for the study of speciation and phenotypic diversification. Some have even gained textbook
status, either due to their sheer extent in terms of species numbers, as for example the African cichlids (e.g.
*Corresponding author. E-mail: [email protected]
Barlow, 2000; Kornfield & Smith, 2000), or because
they have played an important role in the development of modern evolutionary theory, such as the Galapagos finches (e.g. Lack, 1947; Burns, Hackett &
Klein, 2002; Grant & Grant, 2002). In recent years the
application of new molecular techniques such as PCR
or microsatellites have revolutionized the approach to,
and understanding, of some well known radiations
(see, e.g. Givnish & Sytsma, 1997; Sturmbauer, 1998;
Sherbakov, 1999; Schluter, 2000; Burns et al., 2002;
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
513
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T. VON RINTELEN and M. GLAUBRECHT
Salzburger et al., 2002). The correlation of phenotypic
and genetic diversity has proved especially illuminating (see e.g. Sturmbauer & Meyer, 1992; Meyer, 1993
on Lake Victoria cichlids). Deplorably though, while it
has become sufficiently inexpensive and easy to scan
large numbers of species or even populations with
genetic markers, traditional morphological studies
have been neglected at the same time. The latter
approach, however, provides the very data needed to
successfully use molecular results in developing and
testing hypotheses that aim to explain the origin of
organismic diversity and disparity. Accordingly, any
discussion of adaptation and intralacustrine speciation without a solid morphological data basis is at best
incomplete.
Invertebrate radiations, which are much less studied than species flocks in vertebrates, provide the best
examples for this effect. The so-called ‘thalassoid’ (i.e.
marine-like) gastropod assemblage in ancient Lake
Tanganyika is among the best known (see review in
Glaubrecht, 1996). It has been repeatedly (albeit erroneously) cited as a model case of intralacustrine diversification of the pantropical family Thiaridae (Boss,
1978; Michel, 2000; West & Michel, 2000; West et al.,
2003) and compared to other presumed thiarid radiations, for example in Lake Biwa (Japan) and Lake
Malawi (Michel, 1994). Recent anatomical studies
have revealed, however, that all species in Lake Tanganyika previously considered as Thiaridae instead
belong to the Paludomidae (Glaubrecht, 1999; Strong
& Glaubrecht, 2002, 2003; Glaubrecht & Strong,
2004). This finding, which has recently been supported
by molecular data (Wilson, Glaubrecht & Meyer,
2004), renders previous taxonomy-dependent speculations - whether there is, for example, an intrinsic
proneness to radiate in ‘thiarids’ (Michel, 1994) superfluous. In addition, detailed studies of individual
taxa within this species flock, such as Tanganyicia
(Strong & Glaubrecht, 2002) and Stanleya (Strong &
Glaubrecht, 2003) have revealed a far greater diversity of reproductive modes than assumed hitherto. The
implications of these new data for interpretation of the
adaptive radiation of the Lake Tanganyika gastropods
are wide-ranging, given that viviparity has long been
considered one of the decisive factors in molluscan
adaptive radiations in ancient lakes (Cohen &
Johnston, 1987; Johnston & Cohen, 1987; Michel,
1994).
Consequently, in this paper we aim to use a traditional anatomical approach to investigate assumptions about a species flock of live-bearing freshwater
gastropods (Caenogastropoda: Cerithioidea: Pachychilidae) in ancient lakes on the Indonesian island of
Sulawesi (Rintelen et al., 2004) in order to reconcile
morphological data with the most recent molecular
phylogenetic data. This radiation was discovered by
the Swiss naturalists Fritz and Paul Sarasin, who systematically explored most of the island during
research expeditions in 1894–95 and 1902–03, focusing on geology, anthropology and zoology (Sarasin &
Sarasin, 1905). They described 16 new gastropods
endemic to the central lakes and their drainages
(Sarasin & Sarasin, 1897, 1898; Table 1). Later additions (Kruimel, 1913) increased this number by eight,
leading to a total of 24 described snail species. Following the recent description of three new taxa (Rintelen
& Glaubrecht, 2003), and also including riverine taxa,
the total number of pachychilid species currently
known from Sulawesi stands at 34 (see Table 1).
Apart from a brief mention by Sarasin & Sarasin
(1898) of some specimens containing embryonic shells,
hardly any anatomical data were known, with the
exception of operculum and radula descriptions given
for all species then known by Sarasin & Sarasin (1897,
1898) and Kruimel (1913). Although the Sulawesi
pachychilids were not studied in more detail for the
following 80 years, and despite this obvious lack of
data, this lacustrine gastropod flock has since been
cited in only cursory statements as an example of
intralacustrine radiation (e.g. Wesenberg-Lund, 1939;
Brooks, 1950; Davis, 1982). Consequently, ideas developed by these authors on the lacustrine evolution in
Sulawesi suffer from relying on erroneous taxonomybased assumptions. For instance, the species flock in
the two ancient lake systems of the island (Fig. 1) was
thought to comprise two conchologically distinct genera, Brotia H. Adams, 1866 and Tylomelania Sarasin
& Sarasin, 1897 (see Discussion for further details on
the taxonomy of the Sulawesi pachychilids). While
Tylomelania was originally perceived to be endemic,
with four taxa found only in Lake Poso, species of Brotia are widespread not only in Sulawesi but also in
South-East Asia.
The assignment of most Sulawesi pachychilids to
Brotia implicitly led to two assumptions, which are
relevant to evolutionary considerations. First, that
there was a close phylogenetic and biogeographical
relationship of all South-East Asian congeneric taxa
including those on Sulawesi. Second (and deducible
from this), that species of Brotia on Sulawesi, in analogy to known viviparity by means of a subhaemocoelic
broodpouch (i.e. positioned in the neck region of the
head-foot) found in congeneric taxa from the SouthEast Asian mainland (Solem, 1966; Davis, 1971), have
a similar reproductive biology that might facilitate
lacustrine radiation.
Recent studies have revealed both assumptions to
be invalid. Based on the first modern collections made
by Philippe Bouchet (MNHN) in 1991, preliminary
evidence of a rather distinct brooding structure utilizing the pallial gonoduct was found in Sulawesi pachychilids (Rintelen & Glaubrecht, 1999). Meanwhile,
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
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Table 1. Pachychilid species endemic to Sulawesi and their distribution. All species which have not been originally
assigned to Tylomelania (author names in brackets) have been described as ‘Melania’ and were later transferred to Brotia
(see Introduction and Discussion for the reasoning behind their transfer to Tylomelania). Asterisks indicate taxa originally
described as subspecies. The distribution of species endemic to the Malili lakes has not been further specified due to
taxonomic uncertainty at the species level. However, every species in the Malili system is restricted to a single lake or
subset of lakes
Species
Distribution (lake system or region)
Tylomelania abendanoni (Kruimel, 1913)
T. bakara Rintelen & Glaubrecht, 2003
T. carbo Sarasin & Sarasin, 1897
T. carota (Sarasin & Sarasin, 1898)
T. celebicola (Sarasin & Sarasin, 1898)*
T. centaurus (Sarasin & Sarasin, 1898)
T. connectens Sarasin & Sarasin, 1898*
T. gemmifera (Sarasin & Sarasin, 1897)
T. helmuti Rintelen & Glaubrecht, 2003
T. insulaesacrae (Sarasin & Sarasin, 1897)
T. kruimeli Rintelen & Glaubrecht, 2003
T. kuli (Sarasin & Sarasin, 1898)
T. lalemae (Kruimel, 1913)
T. mahalonensis (Kruimel, 1913)
T. mahalonica (Kruimel, 1913)
T. masapensis (Kruimel, 1913)
T. molesta (Sarasin & Sarasin, 1897)
T. monacha (Sarasin & Sarasin, 1899)
T. neritiformis (Sarasin & Sarasin, 1897)
T. palicolarum (Sarasin & Sarasin, 1897)
T. patriarchalis (Sarasin & Sarasin, 1897)
T. perconica (Sarasin & Sarasin, 1898)*
T. perfecta (Mousson, 1849)
T. porcellanica Sarasin & Sarasin, 1897
T. robusta (Martens, 1897)
T. sarasinorum (Kruimel, 1913)
T. scalariopsis (Sarasin & Sarasin, 1897)
T. tominganensis (Kruimel, 1913)
T. tomoriensis (Sarasin & Sarasin, 1898)
T. toradjarum (Sarasin & Sarasin, 1897)
T. towutensis (Sarasin & Sarasin, 1897)*
T. towutica (Kruimel, 1913)
T. wallacei (Reeve, 1860)
T. zeamais (Sarasin & Sarasin, 1897)
Malili lakes
Malili lakes
Lake Poso
Kalaena drainage
Central Sulawesi
Lake Poso
Poso River
Malili lakes
Malili drainage
Malili lakes
Malili lakes
Lake Poso
Malili lakes
Malili lakes
Malili lakes
Malili lakes
Malili lakes
Malili lakes
Poso River
Malili lakes
Malili lakes
Palopo plain
south, south-east and central Sulawesi
Poso River
Toraja region
Malili lakes
Lake Poso drainage
Malili lakes
Tomori area
Lake Poso
Malili lakes
Malili lakes
Maros karst
Malili lakes
parallel research on representatives of Brotia from
other regions in South-East Asia uncovered still different viviparous strategies and reproductive morphologies (Köhler & Glaubrecht, 2001, 2003). We
consequently suggested that the species from
Sulawesi formerly assigned to Brotia and Tylomelania
actually represent an independent pachychilid lineage
distinct from all other South-East Asian taxa (Rintelen & Glaubrecht, 1999; Köhler & Glaubrecht,
2001). In this paper we reassess the evidence for the
existence of two distinct genera within this lineage. In
our anatomical description we have for formal reasons
used Tylomelania for all pachychilid species on
Sulawesi, thus including taxa formerly assigned to
Brotia. This is followed by a discussion of the systematic and biogeographical affinities of the Sulawesi
pachychilids in light of these detailed anatomical
data.
MATERIAL AND METHODS
This study is based on material collected in several
field-trips to Sulawesi in August 1999, March 2000,
September-December 2002 and September -October
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
516
T. VON RINTELEN and M. GLAUBRECHT
A
C
POSO
B
Sulawesi
10 km
MATANO
MAHALONA
LONTOA
TOWUTI
MASAPI
D
100 km
Figure 1. A, Indonesia and Sulawesi. B, Sulawesi and its lakes. C, Lake Poso. D, Malili lake system.
2003. Systematic collections were made in rivers and
streams throughout the distribution area of the
Sulawesi pachychilids and in the ancient lakes as indicated in Table 1 and Figure 13. All material collected
in these field-trips was preserved in 70–95% ethanol.
Voucher specimens employed in this study, including
histological slides and DNA samples, are deposited in
the Malacological Department of the Museum of Natural History, Berlin (ZMB). Locality details and both
museum and GenBank accession numbers for all
sequenced animals are listed in the Appendix. For the
compilation of the distributional data, all accessible
records from the main sampling expeditions to
Sulawesi were evaluated (see caption of Fig. 13).
MORPHOLOGY
Shells were measured to 0.1 mm using an electronic
calliper. Standard shell parameters were taken following Dillon (1984). Embryonic shells were measured
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ANATOMY OF TYLOMELANIA
using an ocular micrometer, and their parameters
taken as in adult specimens.
Anatomy was studied with a stereo-microscope, and
drawings were done with a prisma. Radulae and
embryonic shells were studied by scanning electron
microscopy (SEM). The radula was cleaned enzymatically with proteinase K as described by Holznagel
(1998), sonicated and then mounted on aluminium
specimen stubs with adhesive pads. Embryonic shells
were cleaned mechanically, sonicated, and mounted
on adhesive carbon-coated pads. Both radulae and
embryonic shells were coated with gold-palladium and
studied on a LEO 1450VP scanning electron microscope (software: 32 V02.03) at 10 kV. The dimensions
of the initial whorl of embryonic shells were measured
to 1 mm by SEM using the software. In radulae, teeth
were counted and total radula length measured to
0.1 mm.
HISTOLOGY
Individual parts and organ systems - mainly reproductive organs and head-foot – of selected specimens
were studied histologically. Specimens were embedded
in paraffin using standard procedures. Female gonoducts containing embryonic shells had to be decalcified
in 7% nitric acid (HNO 3) first. Slide sections of 7–
10 mm were stained with haematoxylin/eosine and
embedded in Canada balsam.
MOLECULAR
GENETICS
DNA was purified from about 1–2 mm3 of foot tissue
by CTAB extraction (Winnepenninckx, Backeljau &
De Wachter, 1993). Polymerase chain reaction (PCR)
was used to amplify a ~890 bp region of the mitochondrial 16S ribosomal RNA gene using primers 16SF 5 ¢CCGCACTAGTGATAGCTAGTTTC and H3059 5 ¢-CC
GGTYTGAACTCAGATCATGT (Wilson et al., 2004).
PCR was performed in 25 mL volumes containing 1X
Taq buffer, 1.5 mM MgCl2, 200 mM each dNTP, 1–2.5 U
Taq polymerase, c. 100 nM DNA and ddH2O up to volume on a Perkin Elmer GeneAmp 9600 thermocycler.
After an initial denaturation step of 3 min at 94 ∞C,
cycling conditions were 35 cycles of 1 min each at
94 ∞C, 50–55 ∞C and 72 ∞C, with a final elongation
step of 5 min. The same primers were used in PCR
and sequencing. PCR products were purified with
QiaQuick PCR purification kits (Qiagen). Both
strands of both genes were cycle sequenced using ABI
Prism BigDye terminator chemistry and visualized on
an ABI Prism 377 automated DNA sequencer.
Sequences were aligned with Clustal X 1.8.1 for
Windows (Thompson et al., 1997) using default settings. The resulting alignment was corrected manually. To determine the best substitution model for
517
Bayesian inference analysis (see below), hierarchical
likelihood ratio tests (Posada & Crandall, 2001) were
carried out with MrModelTest 1.1 (Nylander, 2002)
and PAUP*4.0b10a (Swofford, 1998).
Phylogenetic trees were reconstructed by maximum
parsimony using the branch-and-bound algorithm as
implemented in PAUP*, with gaps treated as fifth
base. Support for nodes was estimated by bootstrap
analysis (100 replicates). In addition, Bayesian inference (BI, Huelsenbeck et al., 2001) was employed to
infer phylogeny by using MrBayes 2.01 (Huelsenbeck
& Ronquist, 2001a, b). The MCMCMC algorithm was
run with four independent chains for 250 000 generations, every 100th tree was sampled, and the 1500 first
trees were discarded (burn-in).
Pseudopotamis supralirata (Smith, 1883) was chosen as outgroup to root the phylogeny, because Pseudopotamis has recently been identified as sistergroup of
the Sulawesi pachychilids (see Glaubrecht & Rintelen,
2003).
Museum
ANSP
BMNH
MZB
MNHN
NMB
SMF
ZMA
ZMB
ZMZ
codens
Academy of Natural Sciences, Philadelphia
The Natural History Museum, London
Museum Zoologi, Bogor, Indonesia
Museum d’Histoire Naturelle, Paris
Naturhistorisches Museum, Basel
Senckenberg-Museum, Frankfurt
Zoological Museum, Amsterdam
Museum für Naturkunde, Berlin (formerly
Zoologisches Museum Berlin)
Zoologisches Museum der Universität,
Zürich
Anatomical abbreviations
aa anterior aorta
ag
albumin gland
an anal papilla
ba buccal apparatus
bc
buccal commissure
bg
buccal ganglion
bp brood pouch
bv
blood vessel
cc
cerebral commissure
cg
cerebral ganglion
cp
capsule gland
cpc cerebro-pedal connective
cm columellar muscle
cn
crescentic thickening
cr
crescentic ridge
ct
ctenidium
cv
cardiovascular cavity
dg digestive gland
dgo digestive gland opening
em embryo
er
esophageal roof
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
518
es
ey
ft
gd
gf
gg
gl
go
gp
gs
ht
hy
il
int
kd
lf
ll
mc
me
mf
ml
mo
mr
mu
nd
nt
od
op
os
pg
plg
po
ppc
pr
ra
rd
re
rp
rs
sa
sb
sbg
sbc
sc
sg
sn
spc
srd
ss
st
t1
t2
te
tf
ts
va
T. VON RINTELEN and M. GLAUBRECHT
oesophagus
eye
foot
gonoductal groove
glandular field
genital groove
glabella
pallial gonoduct
glandular pad
gastric shield
heart
hypobranchial gland
intestine loop
intestine
kidney
longitudinal fold
lateral lamina
mantle cavity
mantle edge
mantle fold
medial lamina
mouth
marginal fold
muscle
nidamental gland
nutritive tissue
odontophore
operculum
osphradium
pedal ganglion
pleural ganglion
pallial oviduct
pleuro-pedal connective
posterior pouch (mantle cavity)
radula
radula sac
rectum
nephridial pore
receptaculum seminis
sorting area
spermatophore bursa
suboesophageal ganglion
suboesophageal connective
statocyst
salivary gland
snout
supraoesophageal connective
subradular organ
style sac
stomach
major typhlosole
minor typhlosole
tentacle
transverse folds
testis
vaginal opening
RESULTS
SYSTEMATIC
DESCRIPTION OF
TYLOMELANIA
The anatomical description presented here refers to
all Sulawesi pachychilids as Tylomelania, i.e. including also species currently assigned to Brotia, in anticipation of the Discussion, where evidence from
morphology and molecular genetics for a single pachychilid genus on Sulawesi is evaluated. Whenever, in
contrast, reference is made to Tylomelania sensu Sarasin & Sarasin (1897), this is clearly indicated. Table 1
lists all species-level taxa now included in Tylomelania and their former generic assignment. The description does not include a species-level treatment of taxa,
as a revision is still in progress (T. van Rintelen, P.
Bouchet & M. Glaubrecht, unpubl. data). All data presented are, unless explicitly stated, valid for all species of Sulawesi pachychilids examined so far and not
influenced by taxonomic uncertainties at the species
level. Specimens were assigned to species based on
their shell and radula morphology by a comparison
with the type specimens.
CAENOGASTROPODA COX, 1959
CERITHIOIDEA FÉRUSSAC, 1819
PACHYCHILIDAE TROSCHEL, 1857
TYLOMELANIA SARASIN & SARASIN, 1897
Tylomelania Sarasin & Sarasin, 1897: 317.
Type species: Tylomelania neritiformis Sarasin &
Sarasin, 1897 (subsequent designation by Thiele,
1929)
Diagnosis
Shell globose to highly turreted, usually decollated,
with 3–16 remaining whorls; colour yellowish or
greenish-brown to black; smooth or with fine to strong
axial and/or spiral ribs. Aperture oval, outer lip angulated or round, strong parietal callus in some species;
anterior basis with slight extension. Embryonic shells
with wrinkled sculpture on initial whorl; spiral striae,
axial ribs and sometimes pronounced spiral grooves on
subsequent whorls. Operculum oval to round and multispiral, with a central nucleus.
Head-foot grey or black, rarely yellow, dotted with
white or yellow blotches in some species. Right mantle
edge with broad upward-bound flap on inside. Radula
usually typically pachychilid, very long and coiled at
the posterior right of buccal mass; 2–5 denticles on
marginals. Pallial gonoduct in both sexes open along
its total length, with spermatophore bursa and receptaculum seminis in the female medial lamina. The
species of the genus are ovoviviparous, with the pallial
oviduct containing relatively few but very large juveniles with shells of multiple whorls, i.e. Tylomelania is
a uterine brooder. Very large albumin gland at the pos-
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ANATOMY OF TYLOMELANIA
terior end of the pallial oviduct consists of glandular
folds. Stomach typically pachychilid.
Endemic to Sulawesi, where no other pachychilids
are known to occur.
Description
Shell (Figs 2, 3). Small to very large (adults 10–
117 mm), yellowish-brown, brown or black. Turreted
or elongately conic, in a few species globose, smooth or
with fine to strong axial and/or spiral ribs. The first
whorls usually eroded, often quite heavily, with 3–16
remaining whorls. Oval aperture, holostome, with a
slight extension of the anterior outer lip in most
species.
Operculum (op; Fig. 4B, C). Slightly oval to almost
round, depending on the degree of increase in the last,
smooth and hyaline whorl. Multispiral, with 5–11
whorls around a central nucleus. Ventral side has a
large and round smooth attachment scar of the foot
muscle.
External morphology (Fig. 4). The animal (head-foot)
is grey or black, in some species dotted with irregular
white or yellow blotches, rarely completely yellow. The
broad snout (sn) with the mouth (mo) forms the anterior part of the head, the two tentacles (te) are situated at both sides of its base. The small black eyes (ey)
are on lateral thickenings of the tentacle bases. In
both sexes a genital groove (gg) runs along the foot
along the right side of the head, it ends in a fold
beneath the tentacle.
The posterior two-thirds of the head-foot are covered
by the mantle, the mantle cavity occupies about one to
1.5 coils of the entire animal. The mantle edge (me)
forms a distinct band and is pigmented, in some species its margin is serrated. Well developed papillae as
in some thiarids have not been found. On the right
side of the body an inward fold of the mantle forms a
siphon-like structure (mf, Fig. 5A). This fold is positioned at the anterior end of the pallial gonoduct and
might serve for releasing the gonadal products. The
rectum (re) is visible through the mantle roof. In
brooding females (Fig. 4A, E-L), the embryos (em) can
be seen through the pallium as well, the full brood
pouch (bp) displaces other organs of the pallial cavity
or the immediate postpalliate area considerably, e.g.
rectum and kidney (kd). The stomach (st) occupies
most of the 3rd coil, comprising the intestine loop (il),
style sac (ss) and sorting area (sa) with the crescentic
ridge (cr). The digestive gland (dg) and the gonads
(dorsal) fill the remaining 1–3 coils of the animal. In
males (Fig. 4D), the light coloured and finely grained
testis (ts, see also Fig. 6D) is about as large as the
greenish-brown digestive gland and can easily be distinguished from it. In females, the minute ovary is
branched and barely visible.
519
Pallial organs (Fig. 5A). The pallial organs are the
osphradium (os), the ctenidium (gill, ct), the hypobranchial gland (hy), the rectum (see below, Alimentary system) and the pallial gonoduct (later in this
section).
The white, straight and slender osphradium is
embedded into the pallium; it is only about one third
as long as the ctenidium. The ctenidium consists of
about 80–120 triangular blades; their shape varies
slightly along the gill. An efferent branchial vessel
extends along the posterior part of the gill towards the
heart. The voluminous rectum opens at the mantle
edge with a free anal papilla (an). The long and narrow
hypobranchial gland lies adjacent to the rectum, from
shortly behind the anal papilla to the kidney.
The pallial gonoduct (go) is open, forming a deep
and narrow groove between the medial lamina (ml)
and the lateral lamina (ll, fused with the mantle or
head-foot) in both sexes.
In males (Figs 5C, 6), the medial lamina is a simple
fold without any pouches. The anterior parts of both
laminae are glandular. The nidamental gland (nd) is
formed by a longitudinally grooved glandular pad on
the lateral lamina, and a glandular field (gf) on the
medial lamina consisting of slightly inclined vertical
ridges. The sperm duct enters the pallial gonoduct at
the posterior end where medial and lateral lamina
fuse.
In females (Figs 5A, B, 7, 8), the medial lamina has
a slit-like vaginal opening (va) in the anterior third. A
longitudinal fold (lf) within this opening leads to the
formation of two separate tubes: the ventral receptaculum seminis (rs) and the dorsal spermatophore bursa
(sb); (this interpretation of the dorsal tube is tentative,
as no spermatophores have been found so far in
Tylomelania, see Discussion). The gonoductal groove
is divided by interlocked transverse folds (tf). This
part of the pallial oviduct forms a uterine brood pouch
in adult females, which seems to be formed by the capsule gland (cp). The embryonic shells in the brood
pouch are each embedded in a lump of soft yellowishwhite material between the transverse folds. The
embryos cluster by size within the brood pouch; the
largest one is found most anteriorly (Fig. 4E-L). The
most posterior compartments of the embryo-containing part of the brood pouch hold either only minute
embryos, starting with just 1-2 whorls, or eggs only;
the surrounding tissue is considerably more compact
than in the anterior part. A very large albumin gland
(ag), occupying 10–20% of the whole length of the pallial oviduct, lies posterior to the embryo-containing
section of the brood pouch. The albumin gland is build
by lamellae originating from the lateral and medial
lamella, respectively (Fig. 7G). The lower part forms a
slit-like tube opening to the brood pouch, i.e. the gonoductal groove, if no embryos are present. The ovary
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
520
A
T. VON RINTELEN and M. GLAUBRECHT
C
D
E
F
G
H
U
L
J
B
M
K
N
O
V
P
Q
W
R
X
S
Y
T
Z
Figure 2. Tylomelania, shells (types) of all described lacustrine species. A-G, Lake Poso species. A, T. neritiformis (ST,
NMB 1349a). B, T. connectens (HT, NMB 1335a). C, T. porcellanica (ST, NMB 1347∞). D, T. carbo (ST, NMB 1343a). E,
T. centaurus (HT, NMB 1339a). F, T. kuli (ST, NMB 1329a). G, T. toradjarum (ST, NMB 1328a). H-Z, Malili lake system
species. H, T. insulaesacrae (ST, NMB 1342a). J, T. monacha (ST, NMB 1348a). K, T. zeamais (ST, NMB 1337a). L,
T. gemmifera (ST, NMB 1344a). M, T. masapensis (ST, ZMA). N, T. tominangensis (ST, ZMA). O, T. lalemae (ST, ZMA). P,
T. molesta (ST, NMB 1340a). Q, T. sarasinorum (ST, ZMA). R, T. abendanoni (ST, ZMA). S, T. towutica (ST, ZMA).
T, T. bakara (HT, MZB Gst. 11.956). U, T. kruimeli (HT, MZB Gst. 11.959). V, T. palicolarum (ST, NMB 1331a). W,
T. patriarchalis (ST, NMB 1330a). X, T. mahalonica (ST, ZMA). Y, T. mahalonensis (PLT, ZMA). Z, T. towutensis (PLT, NMB
4790b). Scale bar = 1 cm. HT – holotype, ST – syntype.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
A
B
C
D
E
F
G
H
521
J
Figure 3. Tylomelania, shells (types) of all described riverine species. A, T. perfecta (ST, ZMZ 522348). B, T. robusta (ST,
ZMA). C, T. celebicola (ST, NMB 1333a). D, T. scalariopsis (ST, NMB 1346a). E, T. carota (ST, NMB 1336a). F, T. wallacei
(ST, BMNH 200220115). G, T. tomoriensis (ST, NMB 1345a). H, T. helmuti (HT, MZB Gst. 11.965). J, T. perconica (ST, NMB
3892a). Scale bar = 1 cm. HT – holotype, ST – syntype.
duct enters at the end of the gonoductal groove into
the albumin gland.
Embryonic shells (Fig. 9). The embryonic shells are
relatively large; their size range is 2.8–17.5 mm
(height of largest juvenile within brood pouch) with
2.8–7.5 whorls (N = 32 species). The initial whorl of
the embryonic shells is wrinkled; in some specimens a
transition of sculpture can be seen at about 1.3–1.5
whorls. At c. 2.5 whorls all embryonic shells start to
show a pronounced axial sculpture, even in species
which are smooth as subadults or adults. Two speciesgroups can be distinguished based on whether the
axial ribs on their embryonic shells vanish again after
around two whorls or not (Fig. 9A, B and D, E, respectively). Beside the axial ribs, faint to prominent spiral
grooves may be present. The first whorls of the juveniles can be flat and rounded or high and steep; later
whorls are always straight and angulated. The diameter of the first whorl (d) ranges between 225 and
375 mm (N = 39 species, including yet undescribed
taxa).
Alimentary system. The buccal apparatus (Fig. 10A,
B) immediately behind the mouth (mo) consists of the
muscular (mu) buccal mass containing two jaws, the
subradular organ (srd), and the odontophore (od) supporting the active part of the radula (ra), which is covered by the oesophageal roof (er). The oesophagus (es,
Fig. 10C) exits the buccal mass posteriorly; its anterior section is covered by the large white to pinkish
salivary glands (sg) in the area immediate posterior to
the buccal mass. The long inactive part of the radula is
coiled phonecord-like in the radula sac (rd) to the right
and posterior of the buccal mass. The interior of the
oesophagus is longitudinally folded.
The stomach of Tylomelania (Fig. 10C) has a narrow
and elongate glandular pad (gp), a large and strongly
concave cuticular gastric shield (gs) and a single crescentic ridge (cr). A single opening to the digestive
gland (dgo) is present to the left of the glandular pad,
anterior of the crescentic ridge. The crescentic thickenings (cn) of the sorting area (sa) are present in the
stomach roof; the larger outer crescent has more pronounced septae than the inner one. A marginal fold
(mr) marks the posterior border of the stomach. Intestine (int) and style sac (ss) communicate with each
other, as major and minor typhlosole (t1, t2) are not
fused. A crystalline style is present.
Radula (Fig. 11). The taenioglossate radula is generally very long and robust; the number of tooth rows
per species ranges from 130 to 250 (mean species
values). The maximum length found was 31.7 mm in
T. patriarchalis (Sarasin & Sarasin, 1897). In smaller
species, radula length can exceed shell height (e.g.
21.5 mm vs. c. 15 mm in T. carbo; Sarasin & Sarasin,
1897). A glabella (gl; Fig. 11A; cf. Troschel, 1857) is situated on the front of the central and the lateral teeth;
in the former it resembles a ramp, in the latter a sail.
The rachidian is mostly squarish, with a highly
variable set of denticles (cusps). Denticle arrangement
ranges from a merely slightly enlarged central denticle, flanked by three minor denticles on each side
(Fig. 11A, B), as in almost all other pachychilids from
South-East Asia (Köhler & Glaubrecht, 2001), to an
extremely prominent central denticle (Fig. 11C-F). In
the latter case it can be either squarish or very
pointed, with the minor denticles reduced in size and
number or absent altogether. The upper and lower
margins of the rachidian are concave and convex,
respectively. In some species, two lateral ramp-like
extensions running down from the lateral (minor)
cusps converge towards the glabella. The lateral teeth
are asymmetrical, the size and number of their denticles is correlated to those of the rachidian (cf. Fig. 11).
The marginal teeth are usually to a varying extent
hooked, the number of denticles varies from two to
four on both interior and exterior marginals. The outer
denticles are generally enlarged.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
522
T. VON RINTELEN and M. GLAUBRECHT
A
ag
kd
ey
mf
B
te
dg
C
sn
mo
ft
op
cm
st
cr
re
hy
bp
ts
D
mf
E
dg
mr
st
F
cr
em
J
kd
dg
sa
me
sn
op
ft
ag
G
bp
st
gg
sa
em
re
K
ag
H
L
il
ss
cm
Figure 4. Tylomelania, external morphology and operculum. A, T. sarasinorum, female (ZMB 190129). B, C, opercula,
dorsal. B, T. perfecta (ZMB 190188). C, T. palicolarum (ZMA). D, E, T. perfecta (ZMB 190006). D, male, last coils. E, female.
F-H, T. insulaesacrae, female (ZMB 190160). F, lateral right/dorsal. G, dorsal. H, ventral. J-L, T. palicolarum, female
(ZMB 190153). J, lateral right/dorsal. K, lateral, left. L, ventral. Scale bar = 1 cm.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
A
B
523
C
gf
me
ml
mf
sb
me
an
nd
lf
ct
rs
va
os
ll
rs
sb
ml
re
gd
hy
Figure 5. Tylomelania, pallial organs. A, B, female. A, pallial cavity, dorsal. T. perfecta (ZMB 190086). B, pallial oviduct,
medial lamina. T. patriarchalis (ZMB 190050). C, male. Pallial gonoduct, interior. T. perfecta (ZMB 190086). Scale
bar = 1 mm.
The radulae of two species are highly distinctive.
T. gemmifera (Sarasin & Sarasin, 1897) (Fig. 11G, H;
Lake Matano) and T. kuli (Sarasin & Sarasin, 1898)
from Lake Poso have a very short radula (4–8 mm)
with 20–30 tooth rows per mm, elongated laterals
and unhooked marginals, giving it a thiarid-like
appearance.
Renal system. The highly compartmentalized kidney
lies posterior of the mantle cavity and anterior to the
stomach. The mantle cavity has a pouch-like posterior
extension (pr) with glandular ridges (Figs 6C, 7G),
into which the kidney opens via a nephridial pore (rp,
Fig. 6C).
Nervous system (Fig. 12). The epiathroid nerve system
has a comparatively long cerebral commissure (cc)
and, in contrast, rather short pleuro-pedal (ppc) and
cerebro-pedal connectives (cpc). Cerebral (cg) and
pleural ganglia (plg) are almost fused, the suboesophageal ganglion (sbg) is fused with the left pleural ganglion. The closely joined pedal ganglia (pg) are deeply
embedded into the propodium muscle, covering the
two lateral statocysts (sc), to which they are connected
via short connectives. Seven major nerves branch off
from each of the cerebral ganglia, innervating the
snout (four nerves), tentacle, eye and, via a loopshaped connective, the two buccal ganglia (bg). These
are connected by a suboesophageal buccal commissure
(bc). The anterior aorta (aa) passing through the nerve
ring is very prominent and covers part of the supraoesophageal connective (spc) between the right pleural
and the supraoesophageal ganglion.
Reproductive biology
All examined species of Tylomelania where sex determination was possible are gonochoristic (N = 30 species; N = 2300 individuals). The sex ratio, given as
proportion of males among sexed individuals, ranges
from 0.13 to 0.67 (cf. Table 2), averaging 0.42 overall,
which is a highly significant deviation from a balanced
sex ratio (c2 = 53.261, P < 0.001). In several species or
populations females are significantly larger than
males (Table 3).
On average, around 80% of females (N = 1216) contain embryos in their brood pouch, the number and
size of which vary considerably within and between
species (Table 4). As a rule, larger species have more
and larger embryonic shells in their brood pouch.
Consequently, the largest juvenile has been found in
the largest species, T. patriarchalis, with an embryonic shell height of 17.5 mm in a female of c. 90 mm
(h). In contrast, the largest number of juveniles has
been found in a medium-sized riverine species,
T. robusta, where a female of c. 40 mm (h) contained
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
524
T. VON RINTELEN and M. GLAUBRECHT
A
B
re
kd
ht
mc
bv
bv
cv
go
es
C
D
ts
rp
es
pr
dg
Figure 6. Tylomelania, histological sections of male reproductive organs. T. perfecta (ZMB 190086). Cross-sections, entire
whorl, from anterior to posterior. A, last quarter of pallial gonoduct. B, last fifth of pallial gonoduct. C, immediately
posterior of pallial gonoduct. D, testis and digestive gland, last whorl. Scale bar = 1 mm.
Table 2. Sex ratio in selected Tylomelania species. Only species with respective sample sizes of N = 40 or more sexed
individuals are listed. Population- level sex ratio ranges within one species have been given where at least two populations
with N = 20 or more individuals have been sexed. Chi-square values from an asymptotic c2 test. P = probability value;
values in bold indicate significant deviations from a balanced sex ratio
Species
sex ratio
c2
P
N
T. bakara
T. gemmifera
T. helmuti
T. insulaesacrae
T. kruimeli
T. mahalonensis
T. masapensis
T. patriarchalis
T. perfecta
T. sarasinorum
population level
T. towutensis
population level
T. towutica
T. zeamais
population level
0.55
0.26
0.25
0.39
0.49
0.48
0.25
0.48
0.47
0.48
0.29/0.60
0.49
0.42/0.67
0.39
0.34
0.32/0.46
0.490
31.030
10.000
2.373
0.210
0.190
29.752
0.934
1.344
0.476
–
0.630
–
10.667
30.894
–
0.484
<0.001
0.002
0.123
0.884
0.663
<0.001
0.334
0.246
0.490
–
0.801
–
0.001
<0.001
–
52
134
45
52
51
84
121
243
373
369
21/20
256
132/36
222
315
124/87
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
A
B
rs
525
ll
lf
bp
cp
re
sb
ft
sb
va
rs
C
ml
D
cp
re
nt
tf
bp
re
sb
rs
bp
sb
rs
E
F
sb
sb
rs
rs
G
H
ag
os
bp
ct
re
sb
ey
pr
nt
ba
ht
cv
es
te
bv
kd
em
sb
Figure 7. Tylomelania, histological sections of pallial oviduct. Cross-sections, from anterior to posterior. A-G, T. perfecta
(ZMB 190006). A, section in anterior half of vaginal opening, foot and medial lamina only. B, Last third of vaginal opening.
C, Brood pouch, first third. D, Brood pouch, centre. E, F, brood pouch, last half, section F c. 0.2 mm behind section E. G,
Last fifth of pallial oviduct, at anterior edge of albumin gland. H, T. palicolarum (MNHN). Brood pouch, centre, with
embryo. Scale bar = 1 mm.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
526
T. VON RINTELEN and M. GLAUBRECHT
C
B
D/E
F
G
sb
A
ag
rs
ml
sb
lf
va
tf
ml
ll
sb
rs
lf
ag
va
Figure 8. Tylomelania, schematic reconstruction of pallial oviduct. Pallial oviduct (bottom) and sketches of respective
histological sections (top). Letters correspond to those in Fig. 7. The sections show only the medial lamina (A-F) and the
albumin gland (G), not the whole gonoduct as in the preceding figure.
Table 3. Sexual size dimorphism in Tylomelania. In all
listed species or populations males are smaller than
females. Exclusion from this table does not necessarily
mean that a Tylomelania species shows no sexual size
dimorphism. Besides low sample sizes, taxonomic
confusion may prohibit its statistical detection. h (3
last) = height of three last whorls, h = overall shell height,
F = F-value from a one-factorial ANOVA, P = probability
value; values in bold indicate highly significantly smaller
males
Species
Parameter
T. bakara
T. kruimeli
T. mahalonensis
T. masapensis
T. sarasinorum
ZMB 190123
ZMB 190134
h
h
h
h
h
h
(3
(3
(3
(3
last)
last)
last)
last)
F
P
N
3.667
8.890
7.954
8.137
0.038
0.002
0.007
<0.001
52
60
85
116
10.956
16.895
<0.001
<0.001
48
32
39 juveniles with a maximum embryonic shell height
of 4.8 mm.
A significant correlation between the size of females
and the number of juveniles or the size of the largest
embryonic shell contained in their brood pouch has
been found in 6 and 9 populations, respectively, out of
ten populations with sample sizes of N > 10 juvenilecarrying females tested (Table 5).
There is no evidence of seasonality in reproduction; the proportion of juvenile carrying females
observed within and between the two field-work
periods in August-September 1999 (end of dry season) and March 2000 (end of wet season) remained
unchanged.
Habitat
The species of Tylomelania are either riverine (lotic),
occurring in streams, small rivers and carstic resurgences, or lacustrine (lentic), with relatively many
species in the two central lake systems of Sulawesi. No
riverine species is found in the lakes and vice versa.
Species in the relatively short stretches of river con-
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
A
B
C
D
E
F
527
Figure 9. Tylomelania, embryonic shells. A-C, T. perfecta (ZMB 190008). A, shell, lateral. B, shell, apical. C, protoconch,
apical. D-F, T. matannensis (ZMB 190111). D, shell, lateral. E, shell, apical. F, protoconch, apical. Scale bars = 0.5 mm (A,
B, D, E); = 30 mm (C, F).
necting the Malili lakes (Petea and Tominanga Rivers,
Fig. 1) are considered lacustrine species.
The lotic species often occur in dense populations at
waterfalls in limestone areas. They are confined to
clear water biotopes and seem to be dependent on
large fallen leaves rotting in the water. The snails are
usually found attached to the underside of the leaves,
where they most probably feed on algal films. They
might also feed on the leaves themselves, although
there is as yet no direct evidence of shredding.
The lacustrine Tylomelania species are specific to
either soft or hard substrates, and found on sand and
mud or rocks and sunken wood, respectively, down to
a depth of at least 40 m. Population density is highest in shallow water (1–2 m), especially on rock. In
some cases more than 100 animals per m 2 were
counted. Below -20 m snails become increasingly
scarce. They appear to feed on algae, presumably diatoms, growing on the hard substrate or, to judge from
sand in the rectum, on detritus when dwelling in the
soft substrate.
Distribution
Endemic to Sulawesi with at least 34 species (Fig. 13,
Table 1). Nine riverine species have been found in the
streams and rivers of south, south-east and central
Sulawesi. At least 25 species are endemic to the central lakes (Fig. 1): seven in Lake Poso (including Poso
River) in central Sulawesi, and 18 in the Malili Lakes
(Lakes Matano, Mahalona, Towuti, Lontoa and
Masapi) in the easternmost part of south Sulawesi
(including Tominanga River). Not found in north
Sulawesi. Further details are given in Rintelen (2003).
MOLECULAR
PHYLOGENY
The aligned 16S sequences have a length of 843 bp,
with a very restricted number of short (1–5 bp) and
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
528
T. VON RINTELEN and M. GLAUBRECHT
A
B
C
gs
mo
cn
sn
t2
int
srd
ss
sa
t1
mu
er
od
es
sg
ra
dg
mr
rd
gp
cr
Figure 10. Tylomelania, alimentary system. A, B, T. perfecta (ZMB 190086). A, buccal apparatus. B, buccal apparatus,
detail of anterior section. C, stomach of T. patriarchalis (ZMB 190078). Scale bars = 1 mm.
Table 4. Number and maximum size of embryonic shells in selected Tylomelania species. Only species with respective
sample sizes of N = 10 or more investigated specimens are listed
Number of juveniles
Maximum height of juveniles
Species
Range
Mean
SD
N
Range
Mean
SD
N
T. abendanoni
T. bakara
T. gemmifera
T. helmuti
T. insulaesacrae
T. kruimeli
T. mahalonensis
T. masapensis
T. patriarchalis
T. perfecta
T. sarasinorum
T. solitaria
T. towutensis
T. towutica
T. zeamais
1–4
5–17
1–8
2–15
2–15
2–14
1–11
1–5
2–29
2–23
1–14
1–5
1–8
1–7
1–10
2.6
9.0
4.0
6.0
5.7
7.7
6.0
3.1
5.5
9.8
6.3
3.1
4.9
4.9
4:3
0.93
3.29
2.07
3.25
2.99
3.39
2.99
0.97
4.76
5.07
2.73
1.33
1.84
1.79
1.87
14
21
15
24
15
17
25
77
60
65
57
20
28
15
54
1.0–6.5
6.5–10.0
4.3–9.5
1.0–6.5
2.8–4.5
6.5–11.0
4.0–10.2
0.3–10.0
3.6–17.5
3.0–8.0
0.5–8.5
3.2–10.1
8.5–16.0
0.5–9.3
1.0–7.6
4.9
7.7
7.0
4.9
3.6
8.8
7.9
6.2
9.2
6.4
6.2
7.2
11.7
6.9
5.1
1.38
0.91
1.60
1.30
0.54
1.03
1.33
1.82
2.87
0.89
1.61
1.52
2.30
2.18
1.03
13
21
16
24
11
18
24
77
59
62
50
18
19
15
54
largely unambiguous indels required by the inclusion
of the outgroup sequence (Pseudopotamis supralirata). Of the 135 variable positions, 88 are parsimony informative. Uncorrected distances (p-distance)
range from 0.1 to 17.3% across all sequences (mean
5.2%) and from 0.1 to 5.5% in the Sulawesi pachychilids (mean 3.8%).
The two phylogenetic analyses conducted employing
maximum parsimony (MP) and Bayesian inference
(BI) resulted in identical tree topologies (Fig. 14). The
MP branch-and-bound search recovered six equally
most parsimonious trees with a length of 306 steps
resulting in a fairly well resolved strict consensus cladogram (Fig. 14A). The BI phylogram differs only in
showing a basal polytomy within the Sulawesi pachychilids (Fig. 14B).
While the Sulawesi pachychilids form a monophyletic clade, Tylomelania sensu Sarasin & Sarasin
(1897), comprising the species T. carbo, T. connectens
and T. neritiformis, is shown to be para- or even poly-
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
A
529
B
gl
C
D
E
F
G
H
Figure 11. Tylomelania, radula. A, B, T. perfecta (ZMB 190080). A, segment, frontal. B, segment, apical (45 ∞). C, D,
T. sarasinorum (ZMB 190123). C, segment, frontal. D, segment, apical (45∞). E, F, T. carbo (ZMB 190200). E, segment,
frontal. F, segment, apical (45 ∞). G, H, T. gemmifera (ZMB 190104). G, segment, frontal. H, segment, apical (45 ∞). Scale
bars = 0.1 mm.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
530
T. VON RINTELEN and M. GLAUBRECHT
A
ft
ft
ft
pg
pg
sn bg
plg
sbg
cg
pg
sn
ey
sn
te
sn
ppc
cpc
ft
B
pg
sc
ppc
cpc
plg
cg
cg
sbc
cg
cc
cc
C
sec
es
D
bg
bc
aa
mu
bg
rd
Figure 12. Tylomelania, nervous system. Tylomelania perfecta (ZMB 190086). A, cerebral nerve ring, dorsal view. B,
cerebral nerve ring, ventral view. C, buccal apparatus, left lateral view. D, buccal ganglia, from posterior. Scale bars = 1 mm.
Table 5. Correlation between female shell size and juvenile shell size and number; r = correlation coefficient (Pearson),
P = probability value; values in bold indicate significant correlations
Species
T. bakara
T. masapensis
T. mahalonensis
T. patriarchalis
T. patriarchalis
T. sarasinorum
T. sarasinorum
T. zeamais
T. zeamais
Largest juvenile (shell height)
ZMB
Locality
r
P
r
P
N
190131
190208
190154
190050
190056
190123
190134
190052
190065
Lake
Lake
Lake
Lake
Lake
Lake
Lake
Lake
Lake
0.874
0.564
0.639
0.101
0.285
0.502
0.691
0.113
0.529
0.000
0.000
0.004
0.494
0.268
0.015
0.027
0.533
0.061
0.759
0.421
0.599
0.758
0.556
0.451
0.644
0.818
0.814
0.007
0.000
0.009
0.000
0.031
0.031
0.044
0.000
0.000
11
76
18
47
15
23
10
29
14
Towuti
Masapi
Mahalona
Matano
Matano
Towuti
Towuti
Matano
Matano
phyletic. Its constituent species are found twice in different terminal positions nested within one of the four
major subdivisions.
DISCUSSION
TAXONOMY
Number of juveniles
OF THE
SULAWESI
PACHYCHILIDS
The systematic position of the lake gastropods and
their fluviatile allies remained enigmatic for a long
time. Based on the multispiral operculum with a central nucleus, Sarasin & Sarasin (1898) described all
new species from the central lakes, including Tylomelania, as ‘Palaeomelanien’ in order to distinguish
them from all other ‘melaniids’ found on Sulawesi. The
latter, termed ‘Neomelanien’, have a paucispiral operculum with an excentric nucleus. The Sarasins
regarded both as informal subgroups of ‘Melaniidae’
(see below and Glaubrecht, 1996, 1999 for details of
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
531
100 km
Figure 13. Tylomelania, distribution. Based on material collected by Sarasin & Sarasin (1893-1896, 1902-1903 NMB),
Elbert (Sunda Expedition 1909–1910; SMF), Abendanon (1909-1910; ZMA), NAMRU Expedition (1971–73; ANSP),
Bouchet (1991; MNHN) and the authors (1999, 2000, 2002, 2003; ZMB & MZB).
the recent classification of this group). Seven riverine
species, including the widespread ‘Melania’ perfecta
Mousson, 1849 were also placed in the ‘Palaeomelanien’ based on their operculum. Adding the lake species later described by Kruimel (1913), this group
comprises a total of 31 (sub) species known at that
time (Table 1). Thus Sarasin & Sarasin (1898: 8)
explicitly refrained from the assignment of the ‘Melania’ species among their ‘Palaeomelanien’ to one of the
already named melaniid genera set up for species with
a round and multispiral operculum (e.g. from Asia,
Sulcospira Troschel, 1857, Brotia H. Adams, 1866 and
Pseudopotamis Martens, 1894) as they believed a decision for one of these genera was not possible based on
the data available at the time. They pointed to the
example of South-east Asian Brotia, originally erected
solely based on a multispiral operculum, which is not
a character exclusive to it. The Sarasins noted, however, that the radula of the ‘Palaeomelanien’ was of the
same type as the one described by Troschel (1857) for
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
532
T. VON RINTELEN and M. GLAUBRECHT
A
T. toradjarum
89
T. neritiformis
T. neritiformis
96
T. connectens
96
86
T. gemmifera
96
T. patriarchalis
91
T. zeamais
T. towutensis
99
T. kuli
S
u
l
a
w
e
s
i
T. gemmifera
96
T. zeamais
T. towutensis
99
T. kruimeli
98
T. patriarchalis
91
T. towutica
65
T. porcellanica
T. centaurus
T. centaurus
T. kuli
T. carbo
73
T. toradjarum
99
86
B
T. carbo
65
T. towutica
T. kruimeli
65
T. insulaesacrae
S
u
l
a
w
e
s
i
T. insulaesacrae
98
T. sarasinorum
T. perfecta
T. sarasinorum
T. perfecta
P. supralirata
P. supralirata
10 changes
Figure 14. Tylomelania, molecular phylogeny. Based on 890 bp of the mitochondrial 16SrRNA gene. Grey boxes and taxa
names in bold type indicate the three species of Tylomelania sensu Sarasin & Sarasin (1897, 1898). A, strict consensus
cladogram of six equally most parsimonious trees. Numbers on branches indicate bootstrap support. B, Bayesian inference
phylogram. Numbers on branches are posterior probabilities.
his ‘Pachychili’, one of four groups he distinguished
among the ‘Melaniidae’, comprising Pachychilus Lea &
Lea, 1850 from South America and Sulcospira.
Fischer & Crosse (1892), taking Troschel’s concept
further, divided the ‘Melaniidae’ into six groups, one of
which was the Pachychilinae. Thiele (1921) replaced
the name Pachychilinae, which he erroneously considered to be invalid, with Melanatriinae. These implicitly comprised the ‘Palaeomelanien’ of Sulawesi.
Subsequently, Thiele (1925, 1928, 1929) delimited the
Melanatriinae based on radula and operculum
characters. Köhler & Glaubrecht (2001) replaced
Melanatriinae with the original Pachychilidae. On the
generic level, Thiele (1928) used the similarities of
radula and operculum to assign the Sulawesi species
described as ‘Melania’ to Brotia. He regarded Tylomelania as a subgenus of Sulcospira, again using radula characters, and the parietal callus of the shell
aperture (Thiele, 1929). This in many respects ‘modern’ system, however, was largely ignored by later
authors until recently, and all ‘melanians’ were subsumed under the Thiaridae (e.g. Morrison, 1954).
Based on morphology, the Pachychilidae were
hypothesized to form a monophyletic group outside
the Thiaridae sensu stricto (Glaubrecht, 1996, 1999;
Köhler, Rintelen & Glaubrecht, 2000; Köhler &
Glaubrecht, 2003). Results of a molecular phylogeny
of Cerithioidea (Lydeard et al., 2002) support this
hypothesis, as does a cladistic analysis of morphological data (Glaubrecht, unpubl. data).
For a long time, it has been assumed that the species assigned here to Tylomelania have their closest
relatives among the other South-east Asian pachychilids (see above and Introduction). This assumption
was only made implicitly, however, by the generic
assignation of the two groups then recognized on
Sulawesi - i.e. Tylomelania sensu Sarasin & Sarasin
(1897, 1898) and ‘Melania’ - to the two widespread
South-east Asian genera Brotia and Sulcospira by
Thiele (1928, 1929). For most of the 20th century this
systematic scheme was not challenged; in the worst
case it was simply ignored and the invalid genus ‘Melania’ invoked again (Marwoto, 1997).
The assignment of the Sulawesi pachychilids to
Brotia and Sulcospira was recently challenged on
morphological grounds and the existence of three
independent pachychilid lineages in South-east Asia
recognized (Köhler & Glaubrecht, 2001). Brotia comprises species from the Asian mainland and Sumatra
only, while Sulcospira is confined to Java (Köhler,
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
2003). In contrast, the Sulawesi pachychilids are an
independent lineage, a monophyletic group, based on
both morphological (Rintelen & Glaubrecht, 1999; this
study) and molecular data (Glaubrecht & Rintelen,
2003; this study). Consequently, we suggest extending
the concept of Tylomelania, originally erected for four
taxa endemic to Lake Poso (Sarasin & Sarasin, 1897,
1898), to comprise all pachychilid species on Sulawesi,
thus including taxa formerly assigned to Brotia. This
is based on the following evidence.
Morphology. The description of Tylomelania by Sarasin & Sarasin (1897) is based on two morphological
characters: (1) a globose shell with a parietal callus
and (2) a radula with a single vastly enlarged central
denticle on the rachidian and the lateral teeth (Sarasin
& Sarasin, 1898). The shell - in gastropods in general
and in Sulawesi pachychilids in particular - is highly
variable. Even within Tylomelania (sensu Sarasin &
Sarasin), there is considerable variation. For example,
T. carbo is quite distinct from the other three species.
A comprehensive study of radula morphology in almost
all species of Sulawesi pachychilids, which will be published in the course of a species revision (Rintelen,
Bouchet & Glaubrecht, unpubl. data), has revealed
that the ‘unique’ radula of Tylomelania sensu Sarasin
& Sarasin is well within the interspecific variation
range of the whole Sulawesi species flock (Fig. 11).
Thus, the morphological data render the separation of
a subset of species in a different genus based on these
two characters a rather arbitrary decision.
Soft-part anatomy. All pachychilid species of Sulawesi
have a very similar soft-part anatomy as described
above (Figs 4–12), with virtually no specific differences in qualitative traits at the generic level. Thus,
anatomical characters do not support a subdivision of
the Sulawesi pachychilids.
Molecular genetic data. Although suggesting the existence of several subdivisions within the Sulawesi
pachychilids (Fig. 14), these do not support a clade corresponding to Tylomelania sensu Sarasin & Sarasin
(1897, 1898), which apparently is para- or polyphyletic.
In summary, the Sulawesi pachychilids cannot be
morphologically subdivided without making a highly
arbitrary decision, disregarding the criterion of monophyly, if Tylomelania is restricted to the original set of
species. Alternatively, the erection of several new genera based on the molecular phylogeny would hardly be
supported by morphological characters and would certainly not include Tylomelania in its original sense.
Consequently, all species from Sulawesi formerly
assigned to Brotia are here transferred to Tylomelania, which is the oldest available generic name exclusive to these endemic pachychilids (Table 1). Thus, as
one of three pachychilid lineages in South-east Asia
533
(Köhler & Glaubrecht, 2001, 2003; see below), Tylomelania is the only pachychilid genus in Sulawesi.
Based on molecular data and preliminary morphological findings, the pachychilid genus Pseudopotamis
Martens, 1894 with only two species in the North Australian Torres Strait Islands has recently been proposed as the sister group of Tylomelania (see below;
Glaubrecht & Rintelen, 2003).
COMPARATIVE
AND PHYLOGENETIC ASPECTS OF THE
ANATOMY OF
TYLOMELANIA
General anatomy
The anatomy of Tylomelania as described above is
generally similar to that of all other pachychilid genera (see e.g. descriptions of African Potadoma Swainson, 1840 (Binder, 1959), Malagassy Melanatria
Bowdich, 1822 (Starmühlner, 1969), South American
Pachychilus (Simone, 2001) and the South-east Asian
Brotia and Jagora (Köhler & Glaubrecht, 2001, 2003).
The very different reproductive system is the most
obvious exception and is discussed in detail below.
Of the remaining characters none are possible
autapomorphies of Tylomelania, whose morphology is
dominated by those features that are likely autapomorphies of the Pachychilidae, i.e. symplesiomorphies
at the level discussed here. These include the more-orless round, multispiral operculum with a central
nucleus, the mantle flap on the right side of the headfoot, the pouch-like posterior extension of the mantle
cavity containing the nephropore, the rather long
coiled radula, and the stomach as described above. The
phylogenetic value of characters in the nervous system of Tylomelania is difficult to assess, as a comparative study of pachychilid nervous systems is still
lacking. The only nervous system of a South-east
Asian pachychilid depicted so far, Brotia pageli
(Thiele, 1908), by Köhler & Glaubrecht (2001) does not
seem to differ from that of Tylomelania. This finding
needs to be verified, as do the small differences
between the nervous systems of Tylomelania and
Melanatria (Starmühlner, 1969) in the connection of
the statocysts and nerves branching off from the cerebral ganglia.
Apart from the reproductive system, the only synapomorphy of Tylomelania and its sister taxon Pseudopotamis found so far is a radula with primarily three
marginal denticles (Glaubrecht & Rintelen, 2003; this
study).
Reproductive anatomy and biology
In contrast to all characters mentioned so far, the
female reproductive system of Tylomelania is fundamentally different from that of all other pachychilids
except Pseudopotamis. The sole non-derived character
of this organ complex is the open gonoduct (in both
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
534
T. VON RINTELEN and M. GLAUBRECHT
sexes), a condition which is, however, considered apomorphic for Cerithioidea in general (Glaubrecht,
1996).
The pallial oviduct of Tylomelania is modified to a
uterine brood pouch, a probable synapomorphy with
Pseudopotamis, even though detailed studies of the
latter are still lacking (see below; Glaubrecht & Rintelen, 2003). The modified pallial oviduct of Tylomelania is indeed a complex of several associated derived
characters; these include the apparent modification of
the capsule gland into a compartmentalized brood
pouch, the large albumin gland, and the medial lamina with the specific arrangement of receptaculum
seminis and spermatophore bursa (cf. Figs 5, 7, 8). The
existence of a compartmentalized uterine brood pouch
has been confirmed for Pseudopotamis, while the
arrangement of a spermatophore bursa and receptaculum seminis in the medial lamina as well as an albumin gland might differ from that of Tylomelania
(Glaubrecht & Rintelen, 2003; unpubl. data).
The embryonic shells of Tylomelania are unique
among pachychilids (including Pseudopotamis) in having axial ribs irrespective of adult shell sculpture
(Fig. 9). Their apical whorl has a slightly wrinkled surface typical of several viviparous cerithioideans (see
e.g. Glaubrecht, 1996; Köhler & Glaubrecht, 2001).
However, in contrast to other viviparous pachychilids
such as Brotia and Jagora, there is no evidence for a
retarded formation of the apical shell due to consumption of yolk through the apex, since even the smallest
observable embryonic shells in the brood pouch have a
calcified apex.
As outlined above, the embryonic shells in the brood
pouch of Tylomelania are embedded in nutritive material contained within the egg capsule. The nutritive
function of the tissue can be assessed by comparing
the amount present around the largest, most anterior
embryos (where it is almost gone) and the smaller,
more posterior shells, which are still deeply embedded
in it. Thus, there is no direct transfer of nutrients to
the embryos during their growth period, e.g. through a
histotrophe (see below). Instead, these findings suggest that the huge, conspicuous albumin gland is
responsible for providing the nutrients for development within the egg capsules.
Tylomelania has the largest embryos (size at birth)
among freshwater gastropods (cf. Dillon, 2000: 139)
and possibly all viviparous gastropods. Moreover, the
size range (largest embryo at birth) within Tylomelania exceeds at least that of all other live-bearing cerithioideans as well (Table 6).
Interestingly, no evidence for seasonality in reproduction was observed. Tylomelania species can obviously be long-lived, as suggested by the very large and
strong shells which require some time to build, especially in the oligotrophic lakes of Sulawesi. The ‘layout’
of the brood pouch suggests continuous reproduction,
where only the largest embryos are released. If this
hypothesis could be confirmed, Tylomelania would
have a life-cycle which is very different from that of
other South-east Asian pachychilids, where evidence
for reproductive cohorts was found (Dudgeon, 1982,
1989; Köhler & Glaubrecht, 2003). While ignored in
general treatments of freshwater gastropod life-cycles
(Calow, 1978; Dillon, 2000), some thiarids seem to
reproduce continuously as well (see review in Glaubrecht, 1996). However, data on the life cycle of Tylomelania species are still fragmentary at best. Nothing is
yet known about growth rates, age at maturity and life
span. Equally lacking are data on the paternity of the
embryos, i.e. the question of whether all offspring in a
brood pouch have been sired by one or several males.
The failure to find spermatophores in Tylomelania
(although more than 50 males have been dissected) or
in any other pachychilid, is conspicuous. In the
absence of a penis their presence is, however, highly
likely, which is why pouches in the medial lamina of
the discussed taxa are nevertheless regarded as spermatophore bursae. Among freshwater Cerithioidea an
almost bizarre variety of forms has been described in
the Paludomidae of Lake Tanganyika (Glaubrecht &
Strong, 2004).
Tylomelania is gonochoristic, as are all other Southeast Asian pachychilids, in contrast to earlier suggestions by several authors (see review in Köhler &
Glaubrecht, 2001). While the overall sex ratio deviates
significantly from 0.5 (a completely balanced ratio) in
favour of females, a wide range of ratios was observed
among species and populations (Table 2). A discussion
and comparison of these findings is difficult, as nonrandom sampling in respect to sex cannot be excluded
(cf. criteria given by Dillon, 2000: 109). Females are
often larger than males, and therefore probably more
likely to be collected and examined. This suspicion is
supported by the sex ratios of those species where a
large number of individuals was sexed (e.g.
T. patriarchalis, T. perfecta, T. sarasinorum; Table 2),
which are usually not significantly different from 0.5.
In just one species (T. masapensis) with a highly significantly skewed sex ratio, this is most probably not
an artefact, as the sample was both randomly collected
and examined. If present, the reason for such skewed
sex ratios remains speculative. In other freshwater
gastropods a positive correlation between the proportion of males and the degree of parasite infestation
has been observed (Johnson, 1994; Lively & Johnson,
1994; Dybdahl & Lively, 1996). A similar causation
might be suspected for Tylomelania as well, as some
populations were found to be heavily parasitized.
In contrast to the uterine brooder Tylomelania, Brotia and the closely related Adamietta Brandt, 1974
have a subhaemocoelic brood pouch in the head-foot
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
Littorinidae
Littorina saxatilis
Viviparidae
Viviparus viviparus
GASTROPODS
SELECTED OTHER NON-PULMONATE
CERITHIOIDEA
Marine
Planaxidae
Planaxis sulcatus
Freshwater
Pachychilidae
Adamietta hainanensis
Brotia pagodula
Jagora asperata
Tylomelania insulaesacrae
Tylomelania patriarchalis
Paludomidae
Lavigeria nassa
Potadomoides pelseneeri
Tanganyicia rufofilosa
Tiphobia horei
Pleuroceridae
Semisulcospira libertina
Thiaridae
Hemisinus cf. tuberculatus
Melanoides tuberculata
Tarebia granifera
Thiara scabra
Taxon
matrotroph
matrotroph
matrotroph
matrotroph
subhaemocoel
subhaemocoel
subhaemocoel
subhaemocoel
lecithotroph
lecithotroph
uterine
uterine
lecithotroph
lecithotroph
lecithotroph
lecithotroph
uterine
uterine
mesopodial
uterine
lecithotroph
lecithotroph
lecithotroph
lecithotroph
lecithotroph
lecithotroph
subhaemocoel
subhaemocoel
pallial
uterine
uterine
uterine
nurse eggs
Nourishment
subhaemocoel
Brooding type
(brood pouch)
6–96
10–900
14
15–265
25–74
75–110
6–1016
43
195
68
36
66–248
1–31
275
2–15
2–29
3–4; c. 600*
No. juveniles
4.0
0.4–1.4
2.0–3.0
4.3
3.0
3.4
2.4
1.5
0.4
1.0
3.2
1.0–1.5
3.0–5.6
1.7–2.0
2.8–4.5
3.6–17.5
3.25; 0.5*
SHE
32.0
20.0
37.5
30.0
25.0
19.0
31.0
14.4
10.0
16.0
41.5
34.2
27.4
48.4
14.4
60.8
19.5
AAS
Frömming (1956); Fretter & Graham (1994)
Reid (1996)
Glaubrecht (1996)
Berry & Kadri (1974); Glaubrecht (1996)
Glaubrecht (1996)
Riech (1937); Glaubrecht (1996);
unpubl. data
Davis (1972); Takami (1991)
Glaubrecht, unpubl. data
Glaubrecht & Strong, unpubl. data
Strong & Glaubrecht (2002)
Strong & Glaubrecht, unpubl. data
Köhler & Glaubrecht (2001); Köhler (2003)
Köhler & Glaubrecht (2001); Köhler (2003)
Köhler & Glaubrecht (2003)
this study
this study
Glaubrecht (1996); unpubl. data
Source
Table 6. Diversity of breeding structures and strategies in Cerithioidea. Only species releasing shelled crawling juveniles have been listed. Asterisks indicate the
poecilogonic species Planaxis sulcatus, where numbers separated by a semicolon represent two different reproductive strategies. For the embryonic parameters
the range could not always be given due to lack of data. Abbreviations: SHE, shell height of largest embryo (mm); AAS, average adult shell height
ANATOMY OF TYLOMELANIA
535
536
T. VON RINTELEN and M. GLAUBRECHT
which is very similar in both taxa, while their pallial
gonoducts are distinct (Köhler & Glaubrecht, 2001;
Köhler, 2003). Also in contrast to Tylomelania, all of
these taxa have clearly detectable capsule glands in
the dorsal area of the pallial oviduct where lateral and
medial lamina fuse, and an albumin gland has not
been found. The position of the receptaculum seminis
and spermatophore bursa in the medial lamina of Brotia pageli is analogous to that seen in Tylomelania,
while in the other genera it is not even remotely similar (Köhler & Glaubrecht, 2001). The Philippine
endemic Jagora has a fundamentally different reproductive system again (Köhler & Glaubrecht, 2003). Its
pallial oviduct has a unique arrangement of spermatophore bursa and receptaculum seminis. The position of
the capsule gland is the same as for the other Southeast Asian taxa; in addition, an albumin gland is
present at the posterior end of the gonoduct. Furthermore, it retains egg capsules in the mantle cavity and
provides a rather simple form of brood protection.
The variety of brooding strategies among pachychilids is extraordinary. Three different morphological
solutions have evolved, with two different life-history
strategies (see above). Tylomelania and Pseudopotamis clearly follow a ‘k-strategy’ (MacArthur & Wilson,
1967) and produce comparatively few large embryos
with a lot of reproductive effort devoted to each, while
the other South-east Asian pachychilids generally
have many small juveniles, up to 800 in some species
(‘r-strategy’; see Discussion in Köhler & Glaubrecht,
2001). It should be noted that this comparison of lifehistory traits holds only true within the pachychilids,
while the concept is relative (see Glaubrecht, 1996). In
comparison to some thiarids with a large number of
veligers in the brood pouch (e.g. Stenomelania), all
live-bearing pachychilids are ‘k-strategists’ (Köhler &
Glaubrecht, 2003).
Based on these findings, the homology of the reproductive systems of Tylomelania and the South-east
Asian pachychilid genera must be reassessed. The
general features of the gonoduct are without doubt
homologous (open in both sexes, possession of receptaculum seminis and spermatophore bursa in the
medial lamina), and the respective characters are
symplesiomorphic within the Pachychilidae. The position of the spermatophore bursa and receptaculum
seminis (including their openings within the medial
lamina) and of the gonads and the digestive gland in
the last few body whorls is probably autapomorphic, at
least for each viviparous pachychilid lineage (Köhler,
2003). However, the lack of respective data for some
oviparous taxa (Melanatria, Potadoma) impedes a
more decisive statement. In contrast to the gonoducts,
the brooding structures (as such) of the viviparous
pachychilids are not considered homologous here, in
agreement with findings by Rintelen & Glaubrecht
(1999) and Köhler & Glaubrecht (2001). From a phylogenetic point of view the brooding structures
described above each represent autapomorphies of the
respective taxa. However, the reproductive system,
including the brood pouch of Pseudopotamis, very
likely represents a synapomorphy of that taxon and
Tylomelania, and is indicative of a sister-group relationship of both taxa (Glaubrecht & Rintelen, 2003).
VIVIPARITY
OR OVOVIVIPARITY?
Viviparity has hitherto been used as a synonym for
giving birth to living (shelled) juveniles. However, the
variety of pachychilid breeding structures requires
some clarification of the term, as there are clear differences between the protection of egg capsules in the
mantle cavity (as in Jagora) and the maturation of
juveniles in very large amounts of albumen within the
pallial oviduct (as in Tylomelania). A common criterion of viviparity in a strict sense is the direct nutrient
transfer from the mother animal to the juveniles via a
histotrophe (e.g. Fretter & Graham, 1994: 663), which
is also referred to as matrotrophic viviparity (see,
e.g. Meyer & Lydeard, 1993; Glaubrecht, 1996;
Korniushin & Glaubrecht, 2003). All ‘viviparous’ taxa
in which such direct transfer of nutrients to the growing embryo is lacking are consequently ovoviviparous
(lecithotrophic viviparity).
Accordingly, all pachychilid breeding strategies
discussed here should be regarded as ovoviviparous
(Table 6). No secretive nutritive tissue could be
observed, and the nutrients (albumen) are provided to
the embryo within the egg capsule in all cases, which
are retained within the body (Köhler & Glaubrecht,
2001, 2003; this study). In contrast to earlier assumptions (see review in Glaubrecht, 1996), true viviparity
among Cerithioidea is only found in the Thiaridae
(Table 6; Glaubrecht, 1996, 1999; Köhler & Glaubrecht, 2001). Even within the wider limits of the Caenogastropoda only one other (uncertain) case of true
viviparity can be found (in Janthina; Fretter &
Graham, 1994).
As shown by the variety of brooding structures in
Cerithioidea (Table 6), the term ‘ovoviviparous’ should
not be used to indiscriminately lump together the
wide range of complexity and maternal investment in
the taxa thus subsumed. While ovoviviparous taxa
with more sophisticated reproductive modes (e.g.
Tylomelania or Brotia) may exceed the viviparous
Thiaridae in maternal investment and have structures that are almost as complex, the simple mode
found in Jagora barely surpasses the stage of simple
brood care. Additional terminological distinctions
might thus help to discriminate between such
extremes for certain purposes such as morphological
comparisons. However, for questions of more general
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
biological interest, such as the effect of brooding on
speciation (see next section) the distinction between
matrotrophy and lecithotrophy has been neglected, as
generally the stress is on contrasting the release of
living young (viviparity in a broad sense) and egglaying (oviparity).
VIVIPARITY
AND GASTROPOD RADIATIONS IN
ANCIENT LAKES
Viviparity (including ovoviviparity as differentiated
herein) has frequently been discussed as an important
factor in the diversification of gastropod species flocks
in ancient lakes (reviews in Boss, 1978; Michel, 1994;
Glaubrecht, 1996). It has been claimed for one genus
(Lavigeria) among the 36 gastropod species constituting the Lake Tanganyika flock that slowly dispersing
brooding clades show a higher degree of interpopulation differentiation, even without dispersal barriers,
than non-brooding ones (Cohen & Johnston, 1987;
Johnston & Cohen, 1987). Moreover, the ability to speciate allopatrically seems to be linked with the potential to diversify morphologically as well, as evidenced
by a higher number of sympatric species in Lavigeria
(Michel, 2000; West et al., 2003).
While Tylomelania cannot be employed to test the
effects of brooding on speciation and diversification, as
all species share the same reproductive strategy,
instructive comparisons could potentially be made
with other brooding cerithioidean taxa. Around the
edges of all Sulawesi lakes, thiarids - mainly Tarebia
granifera (Lamarck, 1822) and Melanoides tuberculata (Müller, 1774) - occur in streams and rivers. They
are often syntopic with the widespread fluviatile
Tylomelania perfecta (Table 1). Only T. granifera is
found in a few localities in the lake itself, restricted to
extremely shallow and not very clear water. Both
thiarid species are euviviparous (Table 5; Glaubrecht,
1996, 1999) and parthenogenetic. This finding indicates that rather than the ability to brood, sexual
reproduction or competitive exclusion might be important factors in intralacustrine radiations. Similar
observations can be made in Lake Tanganyika, which
contains only gonochoristic species, while the so-called
radiation of Melanoides in Lake Malawi might provide
a possible exception (Brown, 1994).
BIOGEOGRAPHY
OF THE
SULAWESI
PACHYCHILIDS
As outlined above, the North Australian genus
Pseudopotamis, an endemic with two species on the
Torres Strait Islands, has been proposed as sister
group of Tylomelania based on morphological and
molecular data (Glaubrecht & Rintelen, 2003). The
results of phylogenetic analyses of larger molecular
data sets (Köhler, 2003; Rintelen, 2003) provide
537
almost unanimous support for this hypothesis, confirming the adelphotaxon status of both genera. However, the biogeographical implications of this finding
present a potentially significant problem. Sulawesi
and the Torres Strait Islands are separated by a
2000 km stretch of sea. The present-day pattern must
therefore be explained by invoking either a vicariance
or a dispersal hypothesis.
Vicariance appears to be the obvious choice, as suggested both by the molecular pattern and the presumably extremely low cross-ocean dispersal ability of
these strictly freshwater-dwelling ovoviviparous taxa
(Glaubrecht & Rintelen, 2003). However, in order to
assess the support for a vicariance hypothesis which
might explain a Sulawesi–Australia distribution pattern, the geological background is essential. Sulawesi
is situated in one of the geologically most complex
regions of the world. While it is very difficult for the
non-geologist to fully understand the finer points of
South-east Asian geological history, a basic comprehension of the geological constraints imposed on the
area is crucial to a meaningful interpretation of biogeographical patterns.
South-east Asia consists of Gondwanan fragments
of various ages, which collided with Eurasia in three
sequential events during the Palaeozoic and Mesozoic,
from the Devonian (350 Mya) to the end of the Jurassic (140 Mya) (Metcalfe, 1996, 1998, 2001). During the
Cretaceous, India and Australia separated from Gondwana and moved northwards. The collision of India
with Asia c. 50 Mya caused major deformations in
South-east Asia; these continue to the present day.
Australia’s collision with the Sundaland margin
caused rapid changes in topography in eastern Indonesia and the adjacent West Pacific, especially during
the last 25 Myr (Hall, 1996, 1998, 2001). Thus, geological evolution during the Cenozoic (65 Mya to present)
is of great relevance to biogeographical questions, as
the major tectonic events determining the present configuration of land and sea in the area occurred during
that period (Hall, 2001).
Sulawesi consists of four tectonic provinces with
continental fragments – also referred to as microplates or terranes – at their core (Hall, 1996, 1998;
Moss & Wilson, 1998; Wilson & Moss, 1999). These
provinces are, from west to east: (1) the West Sulawesi
Plutonic-Volcanic Arc, comprising the south arm, the
western part of central Sulawesi and the neck of the
north arm; (2) the Central Sulawesi Metamorphic
Belt, comprising the southern part of the south-east
arm and the middle of central Sulawesi; (3) the East
Sulawesi Ophiolite Belt, comprising the east arm and
the north-eastern part of the south-east arm, and (4)
microcontinental fragments forming the smaller adjacent islands of Banggai and Sula, and the Tukang Besi
group. In addition, there is the volcanic North
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
538
T. VON RINTELEN and M. GLAUBRECHT
Sulawesi Magmatic Arc, comprising the remaining
part of the north arm.
In the following, these tectonic provinces will be
referred to as west-, south-east-, east-, and north
Sulawesi, respectively. The island was formed in the
accretion process of these four fragments to Sundaland from the Cretaceous onward, starting with the
placement of west Sulawesi adjacent to south-east
Borneo. Subsequently, south-east and east Sulawesi
collided with west Sulawesi in the Miocene (20–
15 Mya). Finally, the Banggai-Sula and Tukang Besi
platforms moved close to their present position in the
late Miocene or early Pliocene (8 Mya). The final juxtaposition of these fragments was achieved by internal
rotation through a number of linked strike-slip faults
and thrusts. While the scenario just described is
apparently not very controversial, the distribution of
land and sea on Sulawesi certainly is. According to
Wilson & Moss (1999), Borneo and south Sulawesi
were connected for a few million years in the early
Eocene (c. 50 Mya). In addition, microcontinental fragments of the Tukang Besi and Banggai group might
have been emerged during their passage from the Australian margin towards the rest of Sulawesi, thus suggesting two land migration routes to Sulawesi. Hall
(1998, 2001), however, allows for the presence of land
in south-east Sulawesi from the early Miocene
(20 Mya) but maintains that west Sulawesi was submerged until the late Miocene (10 Mya), with rather
small volcanic islands emerging at best. Towards Australia and the Philippines, island hopping might have
been possible via volcanic island chains about 10–
5 Mya.
The morphological data mentioned above and
genetic data presented by Glaubrecht & Rintelen
(2003) clearly indicate that the Sulawesi pachychilids
do not have their origin in Sundaland. Thus, only one
explanation for the present-day distribution of Tylomelania and Pseudopotamis consistent with the geological facts outlined above remains: a colonization of
Sulawesi from the east on a terrane from the Australian margin (including New Guinea). However, several
severe problems persist. One would expect from this
hypothesis to find that the common ancestor of both
taxa was widely distributed in Australia and/or New
Guinea. However, no pachychilids are found east of
Sulawesi and on the Australian mainland, even
though extensive (if somehow random) sampling has
taken place throughout the area, with the possible
exception of the inner regions of New Guinea. Possibly,
the extinction of pachychilids elsewhere in Australia
(with the exception of the Torres Strait Islands), the
result of drastic climatic changes in the region during
the Pliocene, accounts for the observed pattern (see
review in Glaubrecht & Rintelen, 2003). Consequently,
we have suggested a relict status for Pseudopotamis.
As the Torres Strait Islands were subject to the same
climatic changes, however, the restricted distribution
of Pseudopotamis on them remains enigmatic. A more
critical obstacle is the lack of a geological scenario
hypothesizing an actual, permantly afloat terrane covering the distance between the Australian margin and
Sulawesi (see above). Assuming our biogeographical
hypothesis is valid, there remains a conflict between
the biological and geological data, which cannot be
solved for the time being.
The alternative to vicariance – dispersal - is equally
in conflict with the available data. For a hypothesis,
one of two preconditions must be met. First, animals
would have to have been dispersed across large
stretches of ocean, which is only imaginable by some
agent like birds and hardly testable. Beyond this general difficulty, recent dispersal, e.g. by humans, would
be in conflict with the deep (ancient) split between
Tylomelania and Pseudopotamis evident in the molecular phylogeny presented by Glaubrecht & Rintelen
(2003). Alternatively, the striking similarity in the
reproductive anatomy and biology of Tylomelania and
Pseudopotamis could have developed convergently
after their separation, i.e. their viviparity arose after
the colonization of Sulawesi or the Torres Strait
Islands. The common reproductive characters have so
far been interpreted as homologous and synapomorphic for both taxa, and it does not seem parsimonious
to assume a convergent evolution for both. Even if a
more detailed study of the anatomy of Pseudopotamis
could provide support for an independent origin of viviparity in both taxa, the biogeographical problem outlined above is not eliminated. A dispersal stage able to
survive marine transport is still required, and there is
no evidence for the existence of veliger larvae in
pachychilids so far.
In conclusion, we favour an origin of Tylomelania
following the separation of populations of an ovoviviparous pachychilid ancestor which also gave rise to
Pseudopotamis, as such an hypothesis enjoys better
support from both morphological and molecular data,
and requires far fewer ad-hoc assumptions than a dispersal scenario. The biological data indicate the need
to develop more detailed geological hypotheses on the
movement of plate fragments and their submergence
in the region east of Sulawesi.
ACKNOWLEDGEMENTS
We are very grateful to Ristiyanti Marwoto (MZB) for
her support in arranging the field trips to Sulawesi,
which helped make this study possible. We also thank
LIPI (Indonesian Institute of Sciences) for permits to
conduct research in Indonesia. Invaluable support
was provided by the staff of INCO in Soroako, Lake
Matano. Without their help in providing accommoda-
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
ANATOMY OF TYLOMELANIA
tion, transport and general logistics this study would
not have been such a success.
Philippe Bouchet (MNHN) initiated the study of
Sulawesi pachychilids by visiting the lakes and making all of his material available for a pilot study.
Ambros Hänggi, Urs Wüest (NMB), Robert Moolenbeck (ZMA) and Trudi Meier (ZMZ) are thanked for
their courtesy and generous help with the loan of
material. Ellen Strong shared her anatomical insight.
Nora Brinkmann was immensely helpful with radula
preparation. Thanks also to M. Drescher, S. Schütt, J.
Zeller (ZMB) and A. Munandar (MZB) for technical
assistance. The comments by Ellinor Michel (BMNH)
and one anonymous reviewer helped improve the
manuscript. This study was financed by grants GL
297/1–1/-2, and GL 297/7–1 of the Deutsche Forschungsgemeinschaft (DFG).
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© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542
542
T. VON RINTELEN and M. GLAUBRECHT
APPENDIX
Museum voucher and GenBank numbers of sequenced specimens.
Species
Museum voucher no.
GenBank accession no.
Source
Pseudopotamis supralirata
Tylomelania carbo
T. centaurus
T. connectens
T. gemmifera
T. insulaesacrae
T. kruimeli
T. kuli
T. neritiformis
T. patriarchalis
T. perfecta
T. sarasinorum
T. toradjarum
T. towutensis
T. towutica
T. zeamais
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
ZMB
AY242970
AY311825
AY311830
AY311826
AY242954
AY311858
AY311852
AY311839
AY242960
AY311871
AY242958
AY311906
AY311836
AY311912
AY311924
AY311931
Glaubrecht
this study
this study
this study
Glaubrecht
this study
this study
this study
Glaubrecht
this study
Glaubrecht
this study
this study
this study
this study
this study
190363
190200
190021
190017
190051
190122
190155
190011
190016
190087
190086
190212
190203
190115
190116
190052
& Rintelen (2003)
& Rintelen (2003)
& Rintelen (2003)
& Rintelen (2003)
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 513–542