Kano Y. Vetigastropod Phylogeny (2008)

Vetigastropod phylogeny and a new concept of Seguenzioidea:
Blackwell Publishing Ltd
independent evolution of copulatory organs in the

deep-sea habitats
YASUNORI KANO
Submitted: 31 August 2007 Kano, Y. (2008). Vetigastropod phylogeny and a new concept of Seguenzioidea: independent
Accepted: 31 October 2007 evolution of copulatory organs in the deep-sea habitats. — Zoologica Scripta, 37, 1– 21.
doi:10.1111/j.1463-6409.2007.00316.x Bayesian and maximum-likelihood phylogenies of Vetigastropoda (Mollusca: Gastropoda)
were reconstructed by separate and combined analyses of one mitochondrial (cytochrome
oxidase I, COI) and two nuclear (histone H3 and 18S rRNA) gene sequences, with an emphasis
on dense taxonomic sampling. More than 70 vetigastropod species belonging to 13 families
and 25 subfamilies constituted a robust clade against the two outgroup clades Neomphalina
and Cocculinoidea. The phylogenetically controversial family Seguenziidae appeared as a
derived Vetigastropoda and constituted a highly supported clade with eucycline and cataegine
trochids, and three skeneimorphs (Adeuomphalus, Ventsia and Xyloskenea). These taxa herein
treated as the superfamily Seguenzioidea are morphologically very diverse and grouped only
by the combination of symplesiomorphies in the shell, radular and head-foot characters.
Anatomical peculiarities of Seguenziidae, including the presence of the penis and seminal
receptacle, are all apomorphic conditions independently derived from those in higher gastropod
clades, as a consequence of the small size and in response to deep-sea habitats, where sperm
storage seems to be especially beneficial with low numerical density of individuals and limited
periodic cues for gametogenesis. Indeed, internal or semi-internal fertilization has been
evolved at least six times in Vetigastropoda, essentially in deep-sea lineages, with weak
phylogenetic constraints. Other new vetigastropod clades with high support values include:
Turbinidae + Tegulinae (Trochidae) + Skeneidae s.s., Clypeosectidae + Lepetodrilidae, Anatominae
(Scissurellidae) + Bathyxylophila (Skeneidae) and Lepetodriloidea + Scissurellidae + Bathyxylophila.
Corresponding author: Yasunori Kano, Department of Biological Production and Environmental
Science, University of Miyazaki, 1-1 Gakuen-kibanadai-nishi, Miyazaki 889-2192, Japan. E-mail:
kano@cc.miyazaki-u.ac.jp
Introduction to collect because of the minute sizes, rareness or inaccessibility

Mollusca is arguably the most diverse phylum in the marine of comprising species (e.g. Warén 1991, 1993, 1996; Warén
environment and its species are generally small to minute and & Bouchet 1993, 2001; Kano et al. 2002). On the other hand,
many are very rare, so that assessing the magnitude of the such unusual families and genera (e.g. living monoplacophorans;
richness requires massive collecting efforts (Bouchet et al. Lemche 1957) are important or even essential for under-
2002). Some species are very stenoecious, having highly standing the evolutionary history of molluscan groups. The
specialized habitats or diets or hosts, while others occur quality of molecular phylogenetic analyses, for example,
seasonally or only sporadically, making the determination of largely depends on adequate and sufficient taxon sampling
species richness more problematic. Difficulties also include (e.g. Wallberg et al. 2004).
sampling in environments that are hard to access, like the Vetigastropoda is an archaic group of the class Gastropoda,
abyssal and hadal depths, hydrothermal vents and submarine comprised of several thousands of living species and more
caves where a number of unique species live (e.g. Kase & extinct ones, that have existed since the late Cambrian
Hayami 1992; Warén & Bouchet 1993, 2001; Leal & (Knight et al. 1960). Vetigastropods flourish in the marine
Harasewych 1999). This is also the case for higher taxonomic environment in the widest ranges of depth and latitude, from
categories. Many molluscan families and genera comprise intertidal to hadal zones and from the poles to the equator
only a single or a few species, or they are exceptionally hard (Hickman & McLean 1990; Hickman 1998). They also
© 2007 The Author. Journal compilation © 2007 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 1, January 2008, pp1–21 1
New concept of Seguenzioidea • Y. Kano
inhabit deep-sea hydrothermal vents, and oil and gas seeps The vast diversity of skeneids is represented by only two
and totally dark submarine caves (Warén & Bouchet 1993, species in the sole molecular phylogeny that includes this
2001; Kase & Kano 2002). Mature vetigastropod shells range group (Williams & Ozawa 2006). Other little known families
from minute (0.6 mm) to very large (> 25 cm) and exhibit a include the deep-sea Pendromidae and Ataphridae (Bouchet
variety of shapes and ornamentation including tightly coiled et al. 2005), which have exclusively been treated in limited
conispiral, patelliform, smooth or spined shells (Knight et al. numbers of taxonomic papers (e.g. Warén 1991, 1992).
1960; Ponder & Lindberg 1997). Phylogenetic relationships Adeuomphalus Seguenza, 1876, Sahlingia Warén & Bouchet,
among vetigastropod subgroups have been repeatedly studied 2001 and Mikro Warén, 1996 are also rare deep-sea snails but
using morphological and molecular criteria (e.g. Salvini-Plawan with even more enigmatic systematic positions; only a handful
& Haszprunar 1987; Haszprunar 1988; Hedegaard 1997; of specimens have been caught alive to date and they cannot
Ponder & Lindberg 1997; Sasaki 1998; Colgan et al. 2003; be assigned in a family or a higher taxon within the Veti-
McArthur & Harasewych 2003; Geiger & Thacker 2005; Yoon gastropoda (Warén 1991, 1996; Warén & Bouchet 2001).
& Kim 2005; Williams & Ozawa 2006, review therein). The present paper aims to reconstruct the phylogenetic
The three most recent contributions (Geiger & Thacker frame of Vetigastropoda using multilocus genetic data, putting
2005; Yoon & Kim 2005; Williams & Ozawa 2006) exclusively emphasis on dense taxonomic sampling, with an especial
and extensively deal with the group using larger molecular emphasis on the problematic Seguenziidae and its putative
data sets and provided significant progresses in understanding relatives. Also newly investigated are a number of skeneid and
vetigastropod evolution. The latest phylogeny by Williams other minute snails and limpets from such various marine
& Ozawa (2006) is especially well-organized, recovering a environments as coral reefs and deep-sea floors. The latter
number of newly recognized and highly supported subclades environment includes hydrothermal-vent and sunken-wood
of the group. communities, where a number of phylogenetically and
However, vetigastropod diversity is not yet well-represented ecologically unique organisms have been discovered
in those previous molecular analyses. Recent Vetigastropoda (Marshall 1988; Distel et al. 2000; Little & Vrijenhoek 2003).
contains more than 20 families and dozens of subfamilies,
depending on taxonomic schemes or authors (e.g. Hickman Concept of Vetigastropoda
& McLean 1990; Warén & Bouchet 2001; Bouchet et al. The taxonomic composition of Vetigastropoda remains
2005). Species of many of these families and subfamilies are contentious (Williams & Ozawa 2006). Recent morphology-
hard to collect and to include in molecular analyses, due to based phylogenies and classifications of Gastropoda generally
minute sizes, rareness or inaccessibility (Hickman & McLean recognize the following seven clades: Patellogastropoda,
1990; Warén 1991; Warén & Bouchet 1993, 2001; Geiger Neritimorpha (Neritopsina), Cocculiniformia, Vetigastropoda,
& Thacker 2005). The previous analyses mainly deal with Neomphalina (Hot Vent Taxa), Caenogastropoda and
common, shallow-water, middle- or large-sized species, Heterobranchia (Ponder & Lindberg 1997; Sasaki 1998;
including abalones, turban shells and topshells (e.g. Yoon & Warén & Bouchet 2001). Of these, the definition of Cocculini-
Kim 2005; Williams & Ozawa 2006). formia varies among authors. Cocculiniformia comprises two
Among others, the deep-sea family Seguenziidae is not distinct superfamilies, Cocculinoidea and Lepetelloidea, in
included in any of these analyses, being the most significant the original concept (Salvini-Plawen & Haszprunar 1987;
gap in vetigastropod molecular phylogeny (Geiger & Thacker Haszprunar 1988, 1998). However, Ponder & Lindberg
2005). The importance of the Seguenziidae in understanding (1997) and Sasaki (1998) argued that most characters
the evolution and systematics of Vetigastropoda (and even combining the two superfamilies are plesiomorphic and that
the class Gastropoda) has been stressed with the presence of lepetelloids are derived members of Vetigastropoda. Recent
unique copulatory, circulatory and digestive organs comparable molecular phylogenies including representatives of both
to those in another major gastropod clade, Caenogastropoda. superfamilies also indicate their distant relationship and the
Two morphology-based cladistic analyses recovered Seguenziidae vetigastropod affinity of Lepetelloidea (Colgan et al. 2003;
as one of the first offshoots of Vetigastropoda (Ponder & McArthur & Harasewych 2003). Geiger & Thacker (2005)
Lindberg 1997; Sasaki 1998), while Golikov & Starobogatov instead expanded the taxonomic frame of Vetigastropoda
(1975) place it within the Caenogastropoda. Salvini-Plawen to encompass Cocculiniformia (both Cocculinoidea and
& Haszprunar (1987) and Haszprunar (1988) instead Lepetelloidea) and Neomphalina, based on the shared presence
established its independent order Seguenziina between of bursicles in the gills of the latter hot-vent taxa with
Vetigastropoda and Caenogastropoda. Vetigastropoda in a strict sense (Sasaki 1998), although the
Also neglected is the family Skeneidae, a large polyphyletic monophyly of the three groups has never been suggested in
group of miscellaneous minute snails (Marshall 1988; gastropod phylogenies. The superfamily Seguenzioidea has
Hickman & McLean 1990; Warén 1992; Hickman 1998). even more intricate history of taxonomic treatment, being
2 Zoologica Scripta, 37, 1, January 2008, pp1–21 • © 2007 The Author. Journal compilation © 2007 The Norwegian Academy of Science and Letters
Y. Kano • New concept of Seguenzioidea
variously included in Vetigastropoda and Caenogastropoda shell, operculum, radula and cephalic part of the animal were
or classified in the independent clade Seguenziina (see Ponder kept undamaged in most specimens for future taxonomic
& Lindberg 1997 for review). However, many contemporary studies. Photographs of shells are available from the author
authors place seguenziids within the Vetigastropoda near upon request.
Trochoidea, emphasizing their similarities in tentacle
morphology and shell microstructure (e.g. Bandel 1979; Selection of outgroups
Quinn 1983; Haszprunar 1993; Hickman 1998). Here I included Recent morphological and molecular phylogenies of Gastropoda
Pleurotomarioidea, Haliotoidea, Scissurelloidea, Fissurelloidea, unanimously place Vetigastropoda near Neomphalina (or the
Lepetodriloidea, Trochoidea, Seguenzioidea and Lepetelloidea Hot Vent Taxa; Haszprunar 1988; Sasaki 1998; Colgan et al.
as ingroup taxa, adopting Ponder & Lindberg’s (1997) 2003; McArthur & Harasewych 2003), and the two gastropod
framework. subgroups most probably constitute a monophyletic clade
(see Ponder & Lindberg 1997; Warén et al. 2003). However,
Materials and methods Neomphalina is variously recovered as a paraphyletic grade
Taxonomic sampling in morphological analyses (Haszprunar 1988; Ponder &
Vetigastropod specimens were collected and selected for the Lindberg 1997) or a monophyletic clade in nuclear and
present molecular analysis to increase the total phylogenetic mitochondrial DNA phylogenies (McArthur & Koop 1999;
diversity of operational taxonomic units (OTUs). Results Warén et al. 2003). This group was therefore represented by
from morphology-based classifications were adopted for this both neomphaline families recognized by Warén & Bouchet
purpose (e.g. Quinn 1983; Hickman & McLean 1990; Warén (2001), namely Neomphalidae and Peltospiridae, in the
& Bouchet 1993, 2001; Haszprunar 1998; Hickman 1998), present study. Leptogyra Bush, 1897 and Leptogyropsis Marshall,
and as many recognized families and subfamilies as possible 1988 were also included as the outgroup Neomphalina,
were included in the analysis. Previous molecular studies pro- although the two genera are currently classified in Skeneidae
vided a considerable amount of vetigastropod DNA sequence of Vetigastropoda (e.g. Marshall 1988; Hasegawa 1997). The
data, which well covers the diversity of common intertidal neomphaline affinity of Leptogyra and Leptogyropsis was first
and subtidal groups (e.g. Colgan et al. 2003; Geiger & suggested by Warén & Bouchet (1993) and reinforced with
Thacker 2005; Yoon & Kim 2005). Sample collection was additional conchological and anatomical information now
therefore focused on little known families, subfamilies and available (Kiel & Goedert 2006; G. Haszprunar, personal
genera from various deep-sea environments as well as those communication). Preliminary molecular phylogeny of the
snails and limpets with minute body sizes from shallow seas. Neomphalina indicates their close relationship with
Sequences were newly obtained from 49 vetigastropod Melanodrymia Hickman, 1984 and validity of the family
species representing 10 families and 18 subfamilies (Table 1). Melanodrymiidae (Y. Kano, unpublished data). As outgroup
These include four species of Seguenziidae and nine of their taxa, two species of Cocculinidae (Cocculinoidea) were also
putative relatives (Bouchet et al. 2005) as well as the supposedly included in this study. Cocculinoidea represents the only
polyphyletic Skeneidae (Warén 1992) and enigmatic putative sister group of Vetigastropoda other than Neomphalina
Adeuomphalus with unknown familial status (Warén 1991; (Sasaki 1998; Geiger & Thacker 2005).
Warén & Bouchet 2001). Sequences were also obtained from
the DDBJ/EMBL/GenBank for 26 vetigastropod species, DNA extraction, amplification and sequencing
and the ingroup OTUs represent 13 families and 25 sub- DNA was extracted with Qiagen DNeasy kit from the preserved
families in total. foot and shell muscle tissue. Portions of the mitochondrial
Most live snails were boiled in 70 °C–90 °C water for and nuclear genes, cytochrome oxidase I (COI) and histone
0.1–1 min and the animals were extracted from the shells and H3, were amplified using the primer pairs LCO1490-HCO2198
preserved in pure ethanol. Other snails were relaxed in 7.5% and H3MF-H3MR, respectively (Table 2). PCR reactions
magnesium chloride, or shells were cracked prior to ethanol- were carried out in a final volume of 25 µL [2.5 µL genomic
preservation. Identification of specimens was based on DNA template (c. 100 ng), 17.5 µL ddH2O, 2.5 µL Takara
original descriptions and revisional papers whenever available ExTaq buffer, 2 µL dNTPs (2.5 µM each), 0.2 µL of each
and was in some cases confirmed by Anders Warén and Kazunori primer (20 µM) and 0.1 µL Takara ExTaq enzyme]. After an
Hasegawa. However, many species seemed to be undescribed initial denaturation for 3 min at 94 °C, the reaction solution
and even rigorous assignment to a genus was difficult or were run for 35 cycles with the following parameters:
impossible in several cases. Voucher material has been deposited denaturation for 40 s at 94 °C, annealing for 40 s at gene-
at the Department of Biological Production and Environ- specific temperatures, followed by extension for 60 s at 72 °C.
mental Science, University of Miyazaki, Japan or Muséum Annealing temperatures of 42 °C–45 °C were used for COI
National d’Histoire Naturelle, Paris, France (MNHN). All amplification and 48 °C–54 °C for histone amplification. If
Table 1 Species used in the present analysis, arranged systematically, with DDBJ/EMBL/GenBank accession numbers and collection sites of specimens.
Species COI H3 18S Locality, depth and habitat
(Vetigastropoda)
Pleurotomariidae
Entemnotrochus adansonianus (Crosse & Fischer, 1861) — AY377774 AF120509
Entemnotrochus rumphii (Schepman, 1879) L78911 — —
Perotrochus midas Bayer, 1965 AY296820 AF033709 AF120510
Perotrochus amabilis (Bayer, 1963) AY923929 AY923965 —
Scissurellidae: Scissurellinae
Scissurella sp. cf. coronata Watson, 1885 AY923936 AY923974 —
Sinezona confusa Rolán & Luque, 1994 AF120631 AY377773 AF120512
Scissurellidae: Anatominae
Anatoma sp. A AB365210 AB365260 AB365302 Lau Basin, 1817 m, HV
Anatoma sp. B cf. japonica Adams, 1862 AB365211 — — Izu, Shizuoka, Japan; IN
Haliotidae
Haliotis jacnensis Reeve, 1846 AY923916 AY923952 —
Haliotis tuberculata Linnaeus, 1758 AY377729 AY377775 AF120511
Haliotis virginea Gmelin, 1791 AY923919 AY923955 —
Fissurellidae: Fissurellinae
Macroschisma dilatata (Adams, 1851) AB365212 AB365261 AY335560 Miyazaki, Japan; IN
Fissurellidae: Diodrinae
Diodora cayenensis (Lamarck, 1822) AY377730 AY377776 —
Diodora graeca (Linnaeus, 1758) AF120632 — AF120513
Fissurellidae: Emarginulinae
Emarginula variegata Adams, 1852 AB365213 AB365262 — Okinawa Is., Japan; IN
Montfortula rugosa (Quoy & Gaimard, 1834) AY296819 AF033698 —
Rimula exquisita Adams, 1853 AB365214 AB365263 — Okinawa Is., Japan; IN
Scutus breviculus Blainville, 1817 AB365215 — — Auckland, New Zealand; IN
Scutus unguis (Linnaeus, 1758) AY923912 AY923947 —
Clypeosectidae
Pseudorimula sp. cf. marianae McLean, 1989 AB365216 AB365264 — Lau Basin 1908 m, HV
Lepetodrilidae
Lepetodrilus elevatus McLean, 1988 U56846 AY923959 AY145381
Lepetodrilus pustulosus McLean, 1988 AY923924 AY923960 —
Colloniidae
Homalopoma granuliferum Nomura & Hatai, 1940 AB365217 AB365265 AB365303 Misaki, Kanagawa, Japan; 80 m
Homalopoma maculosa (Pease, 1868) AY923944 AY923982 —
Neocollonia pilula (Dunker, 1860) AB365218 AB365266 — Ibusuki, Kagoshima, Japan; IN
Phasianellidae
Tricolia variabilis (Pease, 1860) AB365219 AB365267 AB365304 Ibaraki, Japan; IN
Turbinidae: Liotiinae
Liotina semiclathratula (Schrenck, 1862) AB365220 AB365268 AB365305 Bonotsu, Kagoshima, Japan; IN (K)
Liotina semiclathratula (Schrenck, 1862) AB365221 — — Tateyama, Chiba, Japan; 70 m (C)
Turbinidae: Turbininae
Astralium calcar (Linnaeus, 1758) AY787400 — —
Astraea undosa (Wood, 1828) AY923941 AY923980 —
Turbo cornutus Lightfoot, 1786 — — AF165311
Turbo setosus Gmelin, 1791 AY923943 AY923981 —
Trochidae: Tegulinae
Norrisia norrisi (Sowerby, 1838) AF080650 — —
Tegula argyrostoma (Gmelin, 1791) AF080658 — AF165311
Tegula eiseni (Jordan, 1936) AF080669 AY923979 —
Trochidae: Margaritinae
Margarites olivaceus (Brown, 1827) AB365222 AB365269 — Hinlopen St., Svalbard, Arctic; 292 m
Trochidae: Stomatellinae
Stomatia phymotis Helbling, 1779 AB365223 — — Ishigaki Is., Okinawa, Japan; IN
Trochidae:Trochinae
Austrocochlea porcata (Adams, 1851) AY296821 — —
Monodonta labio (Linnaeus, 1758) — — X94271
Trochus maculatus Gmelin, 1791 AB365224 AB365270 — Iriomote Is., Okinawa, Japan; IN
Table 1 Continued.
Species COI H3 18S Locality, depth and habitat
Trochidae: Calliostomatinae
Calliostoma sakashitai (Sakurai, 1994) AB365225 AB365271 AB365306 Misaki, Kanagawa, Japan; 80 m
Trochidae: Solariellinae
Minolia punctata Adams, 1860 AB365226 AB365272 — Misaki, Kanagawa, Japan; 80 m
Trochidae: Umboniinae
Umbonium moniliferum (Lamarck, 1822) AB365227 AB365273 — Miyazaki, Japan; IN
Trochidae: Eucyclinae
Agathodonta nortoni McLean, 1984 AB365228 AB365274 — Panglao, Philippines; 300 m
Calliotropis pagodiformis (Schepman, 1908) AB365229 AB365275 AB365307 off Honiara, Solomon Islands; 700 m
Calliotropis sp. cf. abyssicola Rehder & Ladd, 1973 AB365230 — — off Amami Is., Japan; 580 m
‘Calliotropis’ chalkeie Vilvens, 2007 — AB365276 — Malakula, Vanuatu; 600 m
Ginebis argenteonitens (Lischke, 1872) AB365231 AB365277 — Misaki, Kanagawa, Japan; 80 m
Granata lyrata (Pilsbry, 1890) AB365232 AB365278 — Ibusuki, Kagoshima, Japan; IN
Herpetopoma pauperculus (Lischke, 1872) AB365233 — — Ibaraki, Japan; IN
Turcica coreensis Pease, 1860 AB365234 AB365279 — Misaki, Kanagawa, Japan; 80 m
Trochidae: Cataeginae
Cataegis sp. cf. finkli (Petuch, 1987) AB365235 AB365280 AB365308 Malakula, Vanuatu; 780 m
Skeneidae
Bathyxylophila sp. A AB365236 AB365281 AB365309 Espiritu Santo, Vanuatu; 650 m, SW
Bathyxylophila sp. B — AB365282 — French Polynesia; SW
Bruceiella globulus Warén & Bouchet, 1993 AB365237 AB365283 — Lau Basin, 1817 m, HV
Bruceiella? sp. AB365238 AB365284 — Lau Basin 1925 m, HV
Conradia sp. cf. clathrata Adams, 1860 AB365239 AB365285 — Izu, Japan; IN
Dillwynella planorbis Hasegawa, 1997 AB365240 AB365286 AB365310 Kochi, Japan; 150 m, SW
Dillwynella sp. A cf. lignicola Marshall, 1988 AB365241 — — Panglao, Philippines; 300 m, SW
Dillwynella? sp. B AB365242 — — Panglao, Philippines; 70 m, SW
Lodderena sp. AB365243 AB365287 — Izu, Japan; IN
Munditiella ammonoceras (Adams, 1863) AB365244 AB365288 — Ishigaki Is., Okinawa, Japan; IN
Cirsonella sp. A AB365245 — — Chiba, Japan; 90 m, SW
Cirsonella sp. B AB365246 AB365289 — Panglao, Philippines; 70 m, SW
Cirsonella? sp. C AB365247 — — Chiba, Japan; 260 m, SW
Ventsia tricarinata Warén & Bouchet, 1993 AB365248 AB365290 AB365311 Lau Basin, 1817 m, HV
Xyloskenea sp. cf. costulifera Marshall, 1988 AB365249 AB365291 — Solomon Islands; 1100 m, SW
Seguenziidae
Fluxinella sp. cf. polita Marshall, 1991 AB365250 AB365292 AB365312 off Amami Is., Japan; 340 m
Hadroconus sp. cf. altus (Watson, 1879) AB365251 AB365293 — Malakula, Vanuatu; 600 m
Seguenzia sp. A cf. levii Marshall, 1991 AB365252 AB365294 — off Amami Is., Japan; 580 m
Seguenzia sp. B cf. eidalima Marshall, 1991 AB365253 AB365295 — Malakula, Vanuatu; 600 m
Pseudococculinidae
Notocrater pustulosa (Thiele, 1925) AB365254 AB365296 — Ookata, Kochi, Japan; 60 m, SW
Pseudococculinidae sp. A AB365255 AB365297 — Panglao, Philippines; 300 m, SW
Pseudococculinidae sp. B AB365256 AB365298 — Panglao, Philippines; 300 m, SW
Family unknown
Adeuomphalus sp. AB365257 AB365299 — Lau Basin; 1737 m, HV
(Outgroup taxa)
Neomphalina: Neomphalidae
Cyathermia naticoides Warén & Bouchet, 1989 AY923926 AY923962 —
Leptogyra inflata Warén & Bouchet, 1993 AB330998 AB331002 — Lau Basin; 1817 m, HV
Leptogyropsis inflata Hasegawa, 1997 AB365258 AB365300 AB365313 Ibaraki, Japan; 490 m, SW
Neomphalina: Peltospiridae
Depressigyra globulus Warén & Bouchet, 1989 AY296825 AF033689 —
Peltospira delicata McLean, 1989 AY923931 AY923967 —
Rhynchopelta concentrica McLean, 1989 AY923932 AY923968 —
Cocculinoidea: Cocculinidae
Coccopigya punctoradiata (Kuroda & Habe, 1949) AB365259 AB365301 — Miyazaki, Japan; 52 m, SW
Cocculina messingi McLean & Harasewych, 1995 AY377731 AY377777 AF120508
Nomenclature for suprageneric ranks does not reflect result of present phylogeny but tentatively follows Hickman & McLean (1990) and Hickman (1998) with modifications by Warén
& Bouchet (2001) and Williams & Ozawa (2006). Abbreviations: IN, intertidal; HV, hydrothermal vent; SW, sunken wood.
Table 2 Nucleotide sequences of primers

Name Sequence Direction Source
used in this study.
COI
LCO1490 5′-GGTCAACAAATCATAAAGATATTGG-3′ Forward Folmer et al. (1994)
HCO2198 5′-TAAACTTCAGGGTGACCAAAAAATCA-3′ Reverse Folmer et al. (1994)
LCOmod 5′-TCTACTAATCATAAGGAYATYGGNAC-3′ Forward Present study
HCOmod 5′-ACTTCTGGGTGTCCRAARAAYCARAA-3′ Reverse Present study
COIa-NER 5′-CATTTAGTGTAGCAATCAGGRTARTC-3′ Reverse Kano & Kase (2004)
Histone H3
H3MF 5′-ATGGCTCGTACCAAGCAGACTGC-3′ Forward Present study*
H3MR 5′-TGGATGTCCTTGGGCATGATTGTTAC-3′ Reverse Present study*
18S rRNA
18A1 5′-CCTACCTGGTTGATCCTGCCAG-3′ Forward Steiner & Dreyer (2003)
188f 5′-GGATCTATTGGAGGGCAAGT-3′ Forward Present study
NS2 5′-GGCTGCTGGCACCAGACTTGC-3′ Reverse White et al. (1990)
NS5 5′-AACTTAAAGGAATTGACGGAAG-3′ Forward White et al. (1990)
189r 5′-TCGGAATTAACCAGACAAATC-3′ Reverse Present study
1800r 5′-ATGATCCTTCCGCAGGTTCACC-3′ Reverse Steiner & Dreyer (2003)
*Modified from Colgan et al. (2000).
COI amplification was unsuccessful under these conditions, affected only a single OTU were also eliminated. The COI
primers were replaced with the degenerate pairs LCOmod and H3 sequences were aligned by eye in MACCLADE 4.08
and HCOmod, or alternatively, nested PCR strategy was (Maddison & Maddison 2005). All alignments are available
employed using the downstream COIa-NER primer for the upon request from the author.
first run. PCR products were visualized by electrophoresis on Phylogenetic trees were reconstructed from five data sets
1.5% TBE agarose gel, which was stained with ethidium using the Bayesian and maximum likelihood (ML) criteria.
bromide, and photodocumented. Successful PCR products The first three data sets were analysed for the majority of the
were cleaned using ExoSAP-IT (USB) following the described species listed in Table 1 and consisted of two independent
protocol. Both strands were directly cycle-sequenced using COI and H3 gene sequences, and combined data set of the
the amplification primers with a BigDye Terminator v3.1 two genes. The fourth data set consists of the 18S rRNA
Cycle Sequencing Kit (Applied Biosystems, Foster City, CA) sequences from representative species. The fifth data set
on an ABI 310 automated sequencer at University of Miyazaki, concatenated sequences from all the three genes; several
or an ABI 3130 sequencer at the Ocean Research Institute, OTUs were represented by two congeneric species in this
the University of Tokyo. data set. In the Bayesian analyses performed with MRBAYES
Based on phylogenetic trees inferred from the COI and H3 3.1.1 (Ronquist & Huelsenbeck 2003), the general time-
sequences, the complete nuclear 18S rRNA sequences were reversible model was used for all the data sets with invariant
also determined for representative OTUs using 18A1 and site frequency and γ-shape parameter estimated from the data
1800r primers. PCR reactions were carried out with following (GTR + I + G). The shape, proportion of invariant sites,
modifications: annealing temperatures of 54 °C–56 °C and state frequency and substitution rate parameters were
extension time of 90 s. Purified PCR products were sequenced estimated for each codon position separately in the amino
with a range of amplification and internal primers listed in acid coding COI and H3 genes. Each gene was allowed to
Table 2. All sequences have been deposited in the DDBJ/ have different parameters in combined data sets, hence the
EMBL/GenBank with accession numbers in Table 1 fifth data set involving all COI, H3 and 18S genes had seven
(AB365210–AB365313). partitions of parameters. For each data set, two parallel
runs were made for 10 000 000 generations (with a sample
Sequence analysis and phylogenetic reconstruction frequency of 100) using default value of four Markov chains.
Sequences of 18S rRNA gene were aligned using CLUSTALX The first 75 000 trees for each run were discarded to ensure
1.8 (Thompson et al. 1997) at default parameters. Minor the four chains reached stationarity. The consensus tree and
adjustments were then made by eye to conform to the secondary- posterior probabilities (PP) were computed from the remaining
structure models of metazoan small subunit rRNA (Wuyts 50 000 trees (25 000 trees × two runs) in each analysis. PP
et al. 2000). Regions where the alignment was ambiguous equal to or above 95% were considered significant support;
were excluded from the analysis, and sites at which an insertion congruence between individual gene trees was assessed by
looking for conflicting branches with this support. The ML were all recovered as robust monophyletic clades (PP =
analyses were performed for single-gene data sets using 100%). Most congeneric species grouped together, but the
heuristic searches in PAUP* 4.0b10 (Swofford 2002) with strongly supported clade Tegula argyrostoma + Norrisia norrisi
parameter settings identified by using hierarchical likelihood (100%) rendered the genus Tegula paraphyletic. Fourteen
ratio tests implemented in MODELTEST 3.06 (Posada & suprageneric clades of Vetigastropoda received PP support
Crandall 1998). above 95%: Pleurotomariidae (100%), Scissurellinae (100%),
Scissurellinae + Tricolia (96%), Lepetodrilidae + Clypeosectidae
Results (100%), Seguenziidae (100%), Agathodonta + Granata (97%),
Sequence data Ventsia + Xyloskenea (100%), Seguenziidae + Eucyclinae +
Fifty-one partial COI sequences were newly generated and Cataeginae + Ventsia + Xyloskenea + Adeuomphalus (100%),
27 obtained from the DDBJ (78 OTUs in total). The length Emarginula + Montfortula (99%), Emarginula + Montfortula +
of amplified sequences was 658 bp excluding primer regions, Scutus (96%), Fissurellidae except Rimula (99%), Tegulinae
except in two specimens of Liotina semiclathratula, where a (100%), Dillwynella + Cirsonella (98%) and Dillwynella + Cirsonella
6-bp (two amino acids) insertion at positions 98 –103 in the + Bruceiella (100%). The fissurellid clade excluding Rimula
aligned data matrix. This length variant did not appear to but including Macroschisma rendered the subfamily
represent a pseudogene, because neither frameshift nor Emarginulinae (sensu McLean 1984) paraphyletic. The most
termination codons were found, and because most sequence interesting clade in this tree places the Seguenziidae among
substitutions occurred at third codon sites between the two eucycline and cataegine Trochidae, deep-water skeneids
individuals. The 6-bp insertion as well as ambiguous sites Xyloskenea and Ventsia, and enigmatic Adeuomphalus. Trochidae,
near the 5′- and 3′ ends was excluded in the final alignment, Skeneidae and Trochoidea are therefore nonmonophyletic.
resulting in 621 available sites. Of these, 374 characters The ML analysis (GTR + I + G) of the same data produced a
(60%) were variable and 364 (59%) parsimony informative. tree with a similar pattern in shallow branchings (–ln L =
The histone H3 gene tree was constructed with 65 (43 new 22 603.19; not shown). The above 14 clades with significant
and 22 published) partial sequences. The length of amplified PP support were all recovered in the ML tree.
sequences excluding primers was 328 bp in all the species Bayesian analysis of short sequences of the H3 gene
and the alignment had no indels. Ambiguous sites at both resulted in a poorly resolved tree (Fig. 1B). Vetigastropoda
ends were trimmed and 312 sites were included in the final were not recovered as monophyletic; some of the outgroup
alignment, of which 116 (37%) were variable and 106 (34%) taxa constituted a moderately supported clade with Tricolia
were parsimony informative. The combined data set of the and Umbonium (PP = 71%). Only five suprageneric ingroup
COI and H3 had 62 OTUs and 933 (486 variable and 445 clades received significant PP support: Pleurotomariidae
informative) sites. (100%), Scissurellinae (100%), Ventsia + Xyloskenea (99%),
The complete 18S rRNA sequences of 11 vetigastropod Emarginula + Montfortula + Scutus (97%) and Dillwynella +
species amplified in this study range from 1855 bp in Ventsia Cirsonella (99%). The clade consisting of Seguenziidae,
tricarinata and Calliotropis pagodiformis to 1892 bp in Anatoma eucycline and cataegine Trochidae, Xyloskenea, Ventsia and
sp. A (1858 bp in the neomphaline Leptogyropsis inflata) in Adeuomphalus in the COI phylogram was also recovered in
length, including 44 bp of conserved primer sequences. this H3 gene tree but with a lower PP value (81%). The ML
Ten vetigastropod 18S sequences obtained from the DDBJ tree (TrN + I + G, –ln L = 5101.55; not shown) was largely
have similar lengths, except two very long sequences of congruent with the Bayesian tree in topology and it retrieved
Pleurotomariidae (c. 2050 bp). The initial alignment had all of the above-mentioned five clades.
23 OTUs and 2115 sites after exclusion of primer sequences. As the two gene trees were largely congruent in topology,
Twelve alignment-ambiguous regions were also excluded in support for various node were increased in the combined data
the subsequent analyses; most of the excluded 452 ambiguous set of the protein-coding COI and H3 genes (Fig. 2). This
sites were long insertions in pleurotomariids, which were not combined data set indicated Pleurotomariidae as the first
found in other taxa. The final alignment had 1663 sites, of offshoot among the extant Vetigastropoda (100%); this
which 531 (32%) were variable and 302 (18%) were parsimony topology was found in the two independent gene trees but
informative. The combine data set of three genes had 22 with moderate PP support (COI: 89%, H3: 93%). Relationships
OTUs and 2596 (976 variable and 697 informative) sites. of the remaining taxa were uncertain with a large polytomy,
while a number of shallow splits were recovered with high PP
Phylogenetic analyses support. Monophyly of Lepetodrilidae + Clypeosectidae,
The Bayesian analysis of the COI data yielded the tree topology Fissurellidae, Pseudococculinidae, Seguenziidae, Scissurellinae
shown in Fig. 1(A). Vetigastropoda (sensu Ponder & Lindberg and Turbininae were all supported with the highest PP
1997) and the two outgroups Neomphalina and Cocculinoidea (100%). Other significant clades found here but not in the
Fig. 1 A, B. Bayesian phylogenies of vetigastropod molluscs for single gene analyses of (A) mitochondrial COI and (B) nuclear histone H3
genes. Seguenzioidea is newly defined based on results of present study. Numbers above branches denote posterior probabilities; significant
support (≥ 95%) in bold.
Fig. 2 Bayesian phylogeny of vetigastropod

molluscs for combined two-gene analysis of
mitochondrial COI and nuclear histone H3
(933 total sites). Seguenzioidea is newly
defined based on results of present study.
Numbers above branches denote posterior
probabilities; significant support (≥ 95%) in
bold.
individual gene trees include Fissurellidae + Homalopoma (100%). Relationships within the latter group were mostly
(97%) and Calliotropis + Ginebis (100%). The former clade uncertain, owing to very small sequence variation. However,
broke up Colloniidae. some clades have notably long branches and three such clades
The reduced taxon set of the 18S rRNA sequences yielded received the highest PP support: Fissurellidae, Tricolia +
a Bayesian tree shown in Fig. 3(A). The monophyletic Homalopoma and Calliotropis + Cataegis + Ventsia + Fluxinella.
Vetigastropoda were clearly divided into Pleurotomariidae The ML tree (TrNef + I + G; –ln L = 7226.06) concurred in
and remaining families with a large gap between them topology and recovered all the three significant nodes (not
Fig. 3 A, B. Bayesian phylogenies of vetigastropod molluscs for (A) single gene analysis of nuclear 18S rRNA and (B) combined three-gene
analysis of COI, H3 and 18S (2596 aligned sites in total). Seguenzioidea is newly defined based on results of present study. Numbers above
branches denote posterior probabilities; significant support (≥ 95%) in bold.
shown). These results from 18S sequences were incongruent nodes found in the 18S rRNA gene tree. Four significant clades
with those from the COI and COI + H3 data sets in respect were additionally recognized: Anatoma + Bathyxylophila (98%),
of the positions of Tricolia and Homalopoma. However, PP Anatoma + Bathyxylophila + Lepetodrilus + Sinezona (100%),
support for Tricolia + Scissurellinae in the COI tree (Fig. 1A) Ventsia + Fluxinella (95%) and Turbo + Tegula + Dillwynella
and Homalopoma + Fissurellidae in the COI + H3 tree (Fig. 2) (99%). These clades rendered Scissurellidae, Skeneidae and
were relatively low (96% and 97%, respectively), if compared Trochidae all nonmonophyletic.
to the Tricolia + Homalopoma clade in the 18S phylogram
(100%). This incongruence was probably the result of Discussion
saturation in the fast-evolving COI gene. Seguenziidae as a derived member of Vetigastropoda
The Bayesian tree generated from the combined data set of The most important finding of this study is the phylogenetic
the three genes (Fig. 3B) recognized all of the six significant position of the deep-sea family Seguenziidae within the
Vetigastropoda. Seguenziids have a monopectinate ctenidium, phylogeny, while the superfamily Trochoidea (sensu Hickman
a monotocardian heart, male copulatory organ and seminal & McLean 1990) is not recovered as a monophyletic group
receptacle (sperm storage in females) (Ponder & Lindberg by any of the data sets used herein. The nonmonophyly of
1997; Hickman 1998; Sasaki 1998). Such characteristics of Trochoidea has already been pointed out in two multigene
seguenziids are commonly found in Caenogastropoda, and phylogenetic studies (Geiger & Thacker 2005; Williams &
their reduced rhipidoglossate radula resembles caenogastropod Ozawa 2006). Although the 18S rRNA phylogeny by Yoon &
taenioglossate radula in having a lower number of teeth in a Kim (2005) strongly supported the monophyletic Trochoidea,
transverse row (Quinn 1983). On the other hand, protoconch, the group was represented by only four, relatively homo-
faecal pellet morphology and shell structure suggest a geneous subfamilies of Trochidae and Turbinidae in their study.
vetigastropod affinity for the group (Bandel 1979; Quinn Proposed synapomorphies of the group include the presence
1983, 1991; Hedegaard 1997). This mosaic pattern of morpho- of the neck lobes and loss of the right ctenidium and shell slit,
logical traits of the group led Salvini-Plawen & Haszprunar but such characteristics are either reversed or shared with
(1987) and Haszprunar (1988) to place it in the independent other vetigastropod superfamilies (Haszprunar 1988; Hickman
order Seguenziina between Vetigastropoda and Caenogastro- & McLean 1990; Sasaki 1998; see below). The cladistic
poda, and Golikov & Starobogatov (1975) to place it within analysis of shell microstructure also suggested the polyphyletic
the Caenogastropoda. Two morphology-based cladistic nature of Trochoidea (Hedegaard 1997).
analyses (Ponder & Lindberg 1997; Sasaki 1998) similarly
recovered Seguenziidae as a basal clade of Vetigastropoda, Affinity with eucycline and cataegine trochids
perhaps due to its apparent resemblance to caenogastropods, The trochid subfamily Eucyclinae was originally established
cocculinoids and neomphalines in anatomical features. as the independent family Eucyclidae for extinct Mesozoic
However, Quinn (1983) argued that the group has been taxa (Knight et al. 1960). Hickman & McLean (1990) later
derived from an ancestor in Trochoidea, and that its anatomi- adopted the name as a subfamily for both extinct and living
cal peculiarities are all apomorphic conditions independently genera and species. The latter authors recognized three
derived from those in caenogastropods or other clades, as a tribes in Eucyclinae: the extinct Eucyclini (Middle Triassic to
consequence of the small size and in response to a deep-water Oligocene) and extant Chilodontini (Jurassic to Recent) and
habitat. Reduction of body size is often accompanied by Calliotropini (Eocene to Recent). This subfamily was mainly
simplified structures, perhaps via heterochrony. Monopectinate diagnosed by the radular characteristics of the living tribes,
ctenidia are commonly found in the small-sized Scissurellidae including a hooded central tooth with the shaft widening
and Skeneidae (Hickman & McLean 1990; Warén 1992; towards the base, rectangular lateromarginal plate and
Marshall 1993; Ponder & Lindberg 1997; Sasaki 1998). Deep- slender, feathery marginal teeth with finely denticulate cusps
sea members of Vetigastropoda acquired penes and seminal (Hickman & McLean 1990; Hickman 1996).
receptacles several times, presumably as a consequence of Here it is interesting to note that the hooded central and
adaptive evolution to reduce the wastage of gametic products feathery marginal teeth have been found in many species of
in an ecosystem where low numerical density makes locating Seguenziidae (e.g. Ancistrobasis scitula, Marshall 1991: fig. 271;
a mate difficult (Quinn 1983; see below). Seguenzia sp., Hickman 1998: fig. 15.70B) and that the shell
The present molecular data recover seguenziids as a shapes of some eucycline trochids are very similar to those of
derived member of Vetigastropoda, supporting Quinn’s (1983, seguenziids. Rather surprisingly, Bouchet et al. (2005) have
1991) argument. Monophyly of Vetigastropoda (sensu Ponder already proposed a classification of Seguenzioidea and incor-
& Lindberg 1997) and Seguenziidae (here represented by porated eucycline trochids into this superfamily, emphasizing
Seguenzia Jeffreys, 1876, Hadroconus Quinn, 1987 and Fluxinella the similarity between the seguenziid Ancistrobasis Dall, 1889
Marshall, 1983) is strongly supported in the combined analysis and eucycline Calliotropis Seguenza, 1903 in shell morpho-
of the mitochondrial COI and nuclear H3 genes (Fig. 2; logy and external anatomy. Grounds for their classification
PP = 100%). Moreover, analyses of five different data sets also include a 16S rRNA phylogeny for the ‘scaly foot snail’
unanimously identify a novel clade comprising the Seguenziidae, of Neomphalina (Warén et al. 2003), where two outgroup
eucycline and cataegine Trochidae, two deep-sea Skeneidae taxa Seguenzia and Calliotropis were found to form a monophyletic
(Ventsia Warén & Bouchet, 1993 and Xyloskenea Marshall, clade. The present molecular data confirms that various
1988) and the enigmatic Adeuomphalus with unknown familial eucycline trochids including both Calliotropini and Chilo-
status (Figs 1–3). This clade receives 100% PP in all Bayesian dontini are phylogenetically grouped together with seguenziids
phylograms except in the H3 gene tree (PP = 81%), where and that they collectively represent the superfamily Seguen-
phylogenetic signals are not enough strong to support a deep zioidea as proposed by Bouchet et al. (2005). Eucyclinae is the
node with high credibility. The trochoid ancestry of the family first trochid subfamily to appear abundantly in the fossil
suggested by Quinn (1983) is thus approved by molecular record, with a well-developed Triassic and Jurassic history
predating the later Mesozoic or Cenozoic first appearances of Bouchet 1993). The family Skeneidae includes minute snails
other subfamilies (Hickman & McLean 1990). It is therefore with variously shaped, usually colourless shells without the
possible that the Mesozoic eucycline snails represent an inner nacreous or pearly layer. Although most skeneid species
ancestral stock for the Seguenziidae, whose fossil record are represented only by empty shells and very little is known
dates from the Late Cretaceous (Hickman 1998). about their anatomy, the fact that there are so many funda-
The present data is also supportive for the classification of mentally different radular plans in the taxa that have been
Bouchet et al. (2005) in placing the deep-sea genus Cataegis examined is strongly suggestive of their polyphyly (Hickman
McLean & Quinn, 1987 within the Seguenzioidea. Cataegis & McLean 1990; Warén 1992; Hickman 1998). The present
was described as a new subfamily of Trochidae with a peculiar molecular data confirms the close phylogenetic relationship
radular configuration. The radulae examined in the original between Xyloskenea and Ventsia, and their systematic position
description uniformly lacked the central tooth and possess a within the Seguenzioidea (Figs 1 and 2) and accordingly the
fused first pair of laterals (McLean & Quinn 1987). However, polyphyly of Skeneidae.
Warén & Bouchet (1993) illustrated a less modified radula in The species of Adeuomphalus are also minute deep-sea
Cataegis meroglypta that bears the central and lateral teeth of snails but with an even more enigmatic systematic position,
typical trochids. They later found an undescribed species of with only a handful of specimens having been collected
the genus having a eucycline-type of radula (Bouchet et al. alive to date (Warén 1991). These species lack a radula, the
2005), which made them provisionally include Cataegis most useful morphological character in the higher classifica-
within the Seguenzioidea while sustaining the subfamily tion of gastropods, so it has not been possible to assign
Cataeginae in their classification. This independent subfamilial them to a family or a higher taxon within the Vetigastropoda
status may be justified by its anatomical uniqueness including (Warén & Bouchet 2001). Surprisingly, Warén (1991)
the long, dorsal afferent membrane of the ctenidium as well has pointed out that the shell shape and sculpture of
as the lack of the cephalic lappets and right subocular Adeuomphalus are very similar to those of Eudaronia Cotton,
peduncles (McLean & Quinn 1987; Warén & Bouchet 1993: 1945, another little-known deep-sea genus but with a radula,
fig. 15; see below). Chilodontini and Calliotropini were also and this radula resembles those of some seguenziids in having
treated as independent subfamilies (i.e. Chilodontinae and only 11 simple teeth in a transverse row (Warén 1991:
Calliotropinae) and were assigned in the extant family fig. 8A). Nevertheless, he mentioned the possibility of
Chilodontidae together with the Cataeginae, while the convergence during the process of simplifying the teeth
extinct Eucyclini was treated as the independent family (see Warén 1990) and refrained from placing the two genera
Eucyclidae (Bouchet et al. 2005). However, the present near Seguenziidae.
Bayesian trees do not support the monophyly of any The present study shows that Adeuomphalus is certainly
Chilodontidae, Chilodontinae (here represented by Agathodonta related to the latter family and that the radula is a very
Cossmann, 1918; Herpetopoma Pilsbry, 1889 and Granata promising, indicative character for the assignment of skenei-
Cotton, 1957) or Calliotropinae (Calliotropis, Ginebis Taki & form species into the superfamily Seguenzioidea. Many other
Otuka, 1942 and Turcica Adams, 1854). The traditional usage deep-sea genera classified by some authors in Skeneidae have
of trochid subfamilies by Hickman & McLean (1990) is radulae characteristic of seguenziids or eucycline trochids:
tentatively followed in this paper. Akritogyra Warén, 1992; Anekes Bouchet & Warén, 1979,
Benthobrookula Clarke, 1961, Granigyra Dall, 1889; Lissotesta
Skeneimorph genera in Seguenzioidea Iredale, 1915, Moelleriopsis Bush, 1897, Retigyra Warén, 1989,
Xyloskenea, Ventsia and Adeuomphalus are also grouped with Trenchia & Vetulonia Dall, 1913 (see Warén & Bouchet 1989;
seguenziids, and eucycline and cataegine trochids in this Hickman & McLean 1990; Warén 1992, 1993, 1996; Zelaya
newly recognized clade. The genus Xyloskenea, exclusively et al. 2006). Of these, Benthobrookula, Trenchia and Vetulonia
found on sunken pieces of wood in the deep sea, was originally have typical seguenzioid shells and their affinity is unques-
described as a member of Skeneidae (Marshall 1988). Warén tionable. Assignment of the remaining eight genera into
& Bouchet (1993) noted that their new genus Ventsia from the Seguenzioidea is not so conclusive, as their shells do not show
South-Pacific hydrothermal vents is similar to Xyloskenea in any resemblance to any sequenced species of the group,
shell and radular morphology and external anatomy, and also but at least some of them must play important roles in recon-
similar to another deep-sea genus Trenchia Knudsen, 1964 in structing phylogenetic relationships within the superfamily.
radular configuration. The latter authors provisionally The shells of three more genera Palazzia Warén, 1991;
retained Ventsia, Xyloskenea and Trenchia in Skeneidae, while Aequispirella Finlay, 1927 and Brookula Iredale, 1912 likewise
mentioning that the three genera have radulae and shell suggest their seguenzioid affinity, even though the first genus
sculptures resembling those of calliotropine trochids and lacks a radula and the last has been represented exclusively by
therefore likely to be derived from the latter group (Warén & empty shells (Warén 1991, 1992).
Seguenziidae: truly monophyletic?

The three study genera of Seguenziidae (Fluxinella, Hadroconus
and Seguenzia) form a robust clade in the COI tree (Fig. 1A).
However, this taxonomic sampling is not optimal and some
20 genera currently identified in the family may include
phylogenetically heterogeneous taxa. The species of Seguenziidae
have been distinguished morphologically from other veti-
gastropods by the presence of (i) semitubular lobes of mantle
tissue for mantle cavity circulation and corresponding labral
sinuses of the shell aperture; (ii) simplified radula with only
a single pair of lateral teeth in each transverse row; (iii)
monopectinate ctenidium; and (iv) a well-developed penis
posterior to the right cephalic tentacle (Quinn 1983, 1991;
Marshall 1991; Hickman 1998; Sasaki 1998). Of these, the
labral sinuses are the only character used for the familial
assignment of many genera represented exclusively by empty
shells, despite the fact that some taxa (e.g. Basilissopsis
Dautzenberg & Fischer, 1897) lack the sinus but are still
classified as belonging to the family based on their resemblance
to other seguenziids in gross shell morphology (Quinn 1983).
The monopectinate condition of the right gill and the simplified
radula are most probably associated with the reduction of
body size. As mentioned above, many deep-sea skeneimorph
species have radulae similar to those of seguenziids. A Fig. 4 A, B. Critical-point dried animals of eucycline seguenzioid
monopectinate ctenidium has been found in Ventsia and many Granata lyrata from Kagoshima, Japan. —A. Front view of head
other skeneimorphs (Warén 1992; Warén & Bouchet 1993). showing right eye (e), cephalic tentacles (ct) and two different kinds
The boundary is therefore not always clear between seguenziids of ‘subocular peduncles’ (sp1 and sp2). —B. Dorsal view of right eye
and eucycline trochids or skeneimorph seguenzioids. The and a subocular peduncle on right side of eye stalk (sp2), bearing a
ciliated lateral groove (arrows) and a distal ciliary pad (cp) with
penis in males is probably the most distinguishing feature of
unknown function. Abbreviation: cl, cephalic lappet; et, epipodial
the family, although not many species have been investigated
tentacle; nl, neck lobe; sn, snout. Scale bars: 100 µm.
in this context (Quinn 1983, 1991) and a possibly homologous
structure has been found in the hydrothermal-vent eucycline
Bathymargarites (Warén & Bouchet 1989; see below).
condition of the vetigastropod radula is retained to adulthood
New concept of superfamily Seguenzioidea through paedomorphy in Seguenzioidea.
The taxa treated herein as Seguenzioidea are morphologically Although external and internal anatomy is least well-
so diverse that they cannot be defined by a unique, unreversed known for the group, configuration of head-foot tentacles
synapomorphy. Instead, they can be grouped by a series of seems to provide more identification criteria. These criteria
characteristics that have been secondarily modified or lost in include the presence of a peduncle on the right side immediately
some members. For example, their shells are often sculptured posterior to the right cephalic eye. Some eucycline trochids
with reticulate axial and spiral ribs or threads (Hickman 1996: have two projections near the right eye; a smaller one beneath
character 11). However, some species of Seguenziidae (e.g. the eyestalk (Fig. 4: sp1) and a larger one on the right side of
Guttula Schepman, 1908) and skeneimorph Seguenzioidea the stalk (sp2). The former, called right subocular peduncle
(e.g. Eudaronia) have nearly completely smooth shells (Quinn by Crisp (1981), is a rather simple structure found in diverse
1991; Warén 1992). Radular characters are very useful for and presumably unrelated trochoid taxa. Hickman & McLean
identification and many species of the group have a hooded (1990) hence considered that the presence or absence of a
central tooth with the shaft widening towards the base and projection beside the right eye is useless in higher classification
slender, feathery marginal teeth (see Hickman & McLean and phylogenetic inference. Nevertheless, the larger projection
1990: figs 7B, 43 and 47). However, the radula is completely on the right side is present in all eucycline trochids but
lacking in the minute Adeuomphalus and Palazzia. Moreover, absent in other taxa previously classified in Trochidae so far
similar teeth have been found in juveniles of unrelated investigated by the author. The latter projection always
trochoids (Warén 1990), suggesting that a plesiomorphic bears a ciliated lateral groove so that it was once considered
a degraded penis in Calliotropis (e.g. Dall 1889). However, trees and the trochimorph and skeneimorph taxa are left
sexes are separate in this group (e.g. Colman & Tyler 1988; unassigned to families. The phylogeny and evolution of
Hickman 1992), and males and females show identical Seguenzioid families will be discussed more fully elsewhere
morphology as to this projection (Y. Kano, personal observa- (Kano & Warén, in preparation) with the aid of ongoing
tion) except in the hydrothermal-vent genus Bathymargarites, investigations on seguenzioid anatomy (T. Sasaki and T.
where it is hypertrophied in males to actually play a role as an Kunze, personal communication).
intromittent organ (Warén & Bouchet 1989). Regardless of
its unknown function, this posterior peduncle seems to be Other vetigastropod clades
useful in grouping seguenzioids. A similar projection has Besides Seguenzioidea, the present phylogeny retrieves
been described in Seguenziidae (Quinn 1983, 1991), although several well-supported deep nodes that deserve discussion.
a lateral groove has not yet been confirmed in the latter family. These rigorous results include the earliest branching of
On the other hand, topologically comparable projections or Pleurotomariidae within the Vetigastropoda (Figs 1–3), which
peduncles have also been found in very many skeneimorph has already been documented by earlier molecular phylogenies
taxa as well as some members of Fissurellidae and Scissurellidae (Colgan et al. 2003; Geiger & Thacker 2005; Yoon & Kim
(Marshall 1988; Hickman & Mclean 1990; Warén 1992, 1993; 2005; Williams & Ozawa 2006), and the clustering of Colloniidae
Kase & Kano 2002). This is almost certainly because the two and Phasianellidae (Fig. 3), also recovered and discussed in
projections near the right eye are derived ontogenetically Williams & Ozawa (2006). However, there exist new findings
from the two ciliary tentacles found universally in juvenile concerning (i) turbinid affinity of teguline trochids and true
vetigastropods (A. Warén, personal communication; see Ino skeneids; (ii) composition and relationships of lepetodrilids,
1952: pls. 10, 11). Therefore, the projection behind the right clypeosectids and scissurellids; and (iii) within-family relation-
eye is not a synapomorphy of Seguenzioidea, but again a ships of fissurellids. These findings are discussed below
plesiomorphic condition retained in adults perhaps through with reference to our knowledge on their morphology and
paedomorphic evolution. fossil records.
Seguenzioidea includes several hundred species with a The combined three-gene phylogeny (Fig. 3B) clusters
wide range of body size and sometimes with extremely the genera Turbo Linnaeus, 1758, Tegula Lesson, 1835 and
simplified or modified body organization, and this makes the Dillwynella Dall, 1889 with a fairly high (99%) PP. These taxa
above-mentioned characteristics less reliable for the definition are currently placed in the respective families of Turbinidae,
of the group. In contrast, ultrastructural characters, sperm Trochidae and Skeneidae (Table 1; Hickman & McLean
morphology in particular, can be highly conservative and 1990). Turbo is the nominotypical genus of Turbininae and
informative in grouping higher taxa, irrespective of the body Tegula represents Tegulinae; Dillwynella seems to be closely
size or habitat (Healy 1988; Ponder & Lindberg 1997). Previous allied to Skenea Fleming, 1825, the type of Skeneidae. On the
studies on sperm ultrastructure showed that the eucycline contrary, Bouchet et al. (2005) suggest the close affinity of the
genus Calliotropis was fundamentally different from other three groups based mainly on radular morphology and treat
trochoids in having the acrosomal complex deeply implanted them as subfamilies in Turbinidae, namely Turbininae,
within the nucleus (Healy 1989; Hodgson & Foster 1992). Tegulinae and Skeneinae, in their working classification.
This unusual positioning of sperm organelle may reflect The radulae of Tegula and Skenea (and its relatives) are very
the phylogenetic position of Calliotropis distant from other characteristic and similar to those of Turbo in sharing the
trochoids, while it is possibly associated with motility broad central tooth and the mid-shaft bend in the lateral
demands (Healy 1989; see below). Similar conditions may be teeth (e.g. Hickman & McLean 1990: fig. 37; Warén 1992).
found in a wide taxonomic range of seguenzioids, where In fact, Hickman & McLean (1990: 152) admitted that the
sperm ultrastructure has otherwise not been investigated. species of Tegulinae have an unusual distribution of character
In conclusion, the present classification assigns the following states that makes it difficult to justify retaining the subfamily
taxa to the superfamily Seguenzioidea in the superorder within Trochidae rather than transferring it to Turbinidae or
Vetigastropoda based on nuclear and mitochondrial DNA treating it as a separate turbinid derivative. However, they
sequences and morphological criteria: (i) all members of eventually maintained its traditional position in Trochidae
the family Seguenziidae; (ii) all taxa formerly classified in emphasizing the evolutionary conservativeness of conchological
Eucyclinae and Cataeginae of the polyphyletic Trochidae; characters, that is, the oblique aperture and interrupted
and (iii) a number of minute skeneimorph genera that often peristome of the shell and the short growing edge of the
bear seguenziid type of the radula. This result largely concurs operculum in Trochidae. Hickman (1996) later on reconstructed
with a hypothetical working classification of Gastropoda a morphology-based phylogeny of Trochoidea and recovered
proposed by Bouchet et al. (2005). The phylogenetic relation- Tegulinae as the first offshoot of Trochidae that retains the
ship within the superfamily is far from resolved in the present turbinid-like radular conditions as plesiomorphies, but she
also expressed some doubt about the early origin of the group seminal receptacle in Clypeosectus and Lepetodrilus (Fretter
because of its late appearance (Miocene) and later radiation 1988; Haszprunar 1989) also favour the systematic position
(Quaternary) in the fossil record. Likewise, her phylogenetic of clypeosectids in Lepetodriloidea (see below).
analyses retrieved some skeneids within the Turbinidae if The clade Scissurelloidea + Lepetodriloidea was not
radular characters were included (Hickman & McLean 1990: recovered in a previous multigene molecular phylogeny
149). More extensive taxon sampling is required to test the (Geiger & Thacker 2005), where Anatoma was distinguished
close affinity of the three groups and to clarify their phylogenetic from other scissurellids at the familial rank (Anatomidae) as
relationships. the sister taxon of Fissurellidae. This unexpected position of
The three-gene data set also recovers a robust clade Anatoma was probably attributed to a sequence erroneously
composed of Sinezona Finlay, 1926, Lepetodrilus McLean, obtained from a fissurellid species. The COI sequence of
1989; Anatoma Woodward, 1859 and Bathyxylophila Marshall, Anatoma euglypta used therein (AY923934) is nearly identical
1988 (Fig. 3B, PP = 100%) and its subclade consisted of the to that of the fissurellid Montfortula rugosa (AY296819; 0.5%
last two genera (PP = 98%). The close relationship between in uncorrected distance) and fundamentally different (27%–
Sinezona and Lepetodrilus, hence Scissurelloidea and Lepe- 28%) from those of two Anatoma species determined in the
todriloidea, has already been documented by previous molecular present study. Conversely, A. euglypta is more similar to the
phylogenies using 18S rRNA sequences (Yoon & Kim 2005; present Anatoma sp. A in H3 and 18S sequence comparisons
Williams & Ozawa 2006). Most species of Scissurellidae are (8% and 3%, respectively) than to Montfortula (16% and
characterized by symmetrically paired ctenidia and a slit or a 10%). The fast evolving COI gene could have crucial influence
hole (foramen) in the shell, while Lepetodrilidae lack the on the tree topology under the unweighted parsimony criterion
right gill and shell slit or perforation (e.g. Fretter 1988; but used in that study, and independent gene trees were not
see Sasaki 1998 for a reduced right gill in L. nux). This clade reconstructed. Scissurellinae and Anatominae are morpho-
therefore contradicts traditional hypotheses for the gastropod logically closest subfamilies in Scissurellidae (Geiger &
evolution that stress on the importance of symmetry (or Thacker 2005) and the independent familial status for the
asymmetry) in pallial organs including the ctenidium, latter cannot be automatically justified without that molecular
osphradium, hypobranchial gland, kidney and auricle, and support. Contaminated sequence data clearly account for the
resulting presence (or absence) of a shell slit or a foramen unsound 18S tree of archaeogastropod limpets by Schwarz-
through which water is expelled after passing through the paul & Beck (2002).
mantle cavity (see Lindberg & Ponder 2001 for review). The The combined COI and H3 tree identifies three consistent
pallial organs at the right side have been repeatedly lost in clades within the Fissurellidae (Fig. 2). Fissurellid limpets
vetigastropod evolution. Among scissurellid subfamilies, the traditionally have been treated under three subfamilies,
Larocheinae have only the left, monopectinate ctenidium namely Fissurellinae, Emarginulinae and Diodorinae, based
and a slit-less shell (Marshall 1993; Kase & Kano 2002). on the shell shape and radula (Hickman 1998), although some
Bathyxylophila seems to be another scissurellid with a single authors emphasize the taxonomic importance of radular
ctenidium (Fig. 3B), regardless of its current position in characters and synonymize Diodorinae under Emarginulinae
Skeneidae (Table 1). The shell and radula of Bathyxylophila (McLean 1984; Sasaki 1998). In the combined two-gene tree,
resemble those of Larochea Finlay, 1927, the type of Larocheinae, Emarginulinae represents the basal grade and each Fissurellinae
as already noted in the original description of the former (here represented by Macroschisma Sowerby, 1839) and
genus (Marshall 1988). Diodorinae (Diodora Gray, 1821) appears as a terminal
The confident clustering of Lepetodrilus and clypeosectid branch of the family. This topology disputes both of the
genus Pseudorimula McLean, 1989 by the COI and H3 data above subfamilial classifications, but concurs well with the
(Figs 1 and 2) further shows the evolutionary plasticity of the Triassic origin of Emarginulinae and much more recent
paired state of the pallial complex. Clypeosectidae (Clypeosectus (Cenozoic) appearance of the latter two subfamilies in the
McLean, 1989 and Pseudorimula) had been placed near fossil record (McLean 1984). The same tree also challenges
Fissurellidae in the superfamily Fissurelloidea, based on the the proposed evolutionary trend of shell characters. Fissurellid
patelliform shell with an anterior slit, paired gill and a few shell modifications for exhalent discharge range from a
other anatomical characteristics found consistently (but not shallow anterior notch to a relatively deep slit to a foramen
exclusively) in the two families (Haszprunar 1989; McLean located on the anterior slope or apex (Hickman 1998); of
1989). However, Warén & Bouchet (2001) put Clypeosectus these, the notch and slit are considered to be plesiomorphic
and Pseudorimula into Lepetodrilidae because of their and the foramen to be a derived condition (McLean & Geiger
similarity to Lepetodrilus in the shape of the protoconch and 1998). However, three study genera with the shell notch or
radula (Bouchet et al. 2005). The presence of apparently slit (Scutus Montfort, 1810, Montfortula Iredale, 1925 and
homologous copulatory organs including the penis and Emarginula Lamarck, 1801) constitute a robust monophylum,
which is sister to the moderately supported (PP = 94%) clade
Table 3 Vetigastropod lineages with independently developed male intromittent organs (penes), female sperm-storage (seminal receptacles) and/or hermaphrodism. Seguenziidae and
Sublittoral to hadal (mainly bathyal)e–g

Bathyal to abyssal; hydrothermal ventb
References: aFretter (1988), bWarén & Bouchet (2001), cHaszprunar (1989), dSasaki (1998), eMarshall (1985), fHaszprunar & McLean (1996), gHaszprunar (1998), hQuinn (1983), iMarshall (1983), jHickman (1998), kWarén & Bouchet (1989),
Sublittoral to hadal (mainly bathyal)h–j
Diodora + Macroschisma with the apical hole. The earliest
branching of Rimula Defrance, 1827 with a foramen on the
Abyssal; hydrothermal ventb
Abyssal; hydrothermal ventb

anterior slope of the shell therefore suggests that the foramen
Depth range and habitat
Intertidal to abyssall–n
has acquired more than once in this family, or alternatively,
Sublittoral to bathyall
the slit may have re-evolved from the foramen.
Multiple origins of copulatory and sperm-storage organs in

Vetigastropoda
Most vetigastropods employ external fertilization, often
simply releasing gametes into the water. In contrast, internal
Gonochoristic or hermaphroditef,g
Simultaneous hermaphroditel,m
fertilization, with correlated changes in both male and female
reproductive systems, is consistently found in derived gastropods
including Neritimorpha, Caenogastropoda and Heterobranchia
Gonochoristica–d
(Ponder & Lindberg 1997). Seguenziidae has traditionally
Gonochoristicd,h
a
Gonochoristick
Gonochoristicl
Gonochoristic
been regarded as an enigmatic group in having copulatory
organs and other traits found mainly in Caenogastropoda,
Sex
and at the same time, morphological features confined to
Vetigastropoda (see above). However, the present molecular
phylogeny clearly shows a derived position of Seguenziidae
Left side of inner pallial wall (if present)f,g

within the Vetigastropoda and suggests a relatively recent
origin for the penis and seminal receptacle. Anatomical,
Right side of inner pallial walld

Position of seminal receptacle
Left side of inner pallial walld
Left side of inner pallial walll

histological and spermatological studies in the last two decades
have, in fact, revealed that reproductive organs and (semi-)
internal fertilization are not rare among vetigastropods
inhabiting various deep-sea ecosystems (Table 3). Here I
review the morphological characteristics and phylogenetic
No data
No data
a
and ecological distributions of these organs in relation to Absent
Bathymargarites may constitute a clade and their male organs are possibly homologous.
their adaptive significances. Available knowledge of sperm

morphology, which in part reflects the type of fertilization, is
Ventral base of right cephalic tentaclea–c
also provided for taxa with possible copulatory behaviour.

Right cephalic tentacle (if present)e–g
Among the taxa with copulatory and/or sperm-storage Anterior right corner of footl–n
organs, the hydrothermal-vent limpet Lepetodrilidae represents
Right subocular pedunclek
Origin or position of penis
a relatively well-documented example, both in morphological

and ecological aspects. Fretter (1988) described the anatomy
a
Left wall of snout
Right neck lobeh
and histology of five species of Lepetodrilus in great detail,

showing that the male bears a penis at the ventral base of the
No data
right cephalic tentacle with an open seminal groove. The

Warén (1991), mWarén (1992, 1993), nWarén & Bouchet (1993).
female has a seminal receptacle at the right side of the inner

pallial wall (see also Warén & Bouchet 2001: fig. 20a; Kelly
Skeneidae s.s. (seven genera)l–n
& Metaxas 2007). She found no direct connection between

Lepetodrilus, Clypeosectus
the receptacle and oviduct, and therefore argued that mature

ova are fertilized in the mantle cavity of the female, employing
semi-internal fertilization (Fretter 1988). Ultrastructural
Bathymargarites
Family or genus
Seguenziidae
Pendromidae
investigation of sperm morphology supports this argument.

Gorgoleptis
All families
Lepetodrilus produces ‘ent-aquasperm’, which are initially

shed into the water but fertilize the egg inside the female, but
not the ‘ect-aquasperm’ typical for vetigastropods with external
fertilization (Hodgson et al. 1997). The penis and receptacle
Lepetodriloidea
Lepetodriloidea
Seguenzioidea
Seguenzioidea
Lepetelloidea
‘Trochoidea’
‘Trochoidea’
found in another vent limpet genus Clypeosectus (Haszprunar

Superfamily
1989) are apparently homologous to those of Lepetodrilus in

view of their topology and morphology, regardless of their
l
current taxonomic positions in different families. The ventral supposed terminal clade of the group (Haszprunar & McLean
base of the right cephalic tentacle is not a common position 1996), may have evolved by reversal, or alternatively, independent
for gastropod penes (Ponder & Lindberg 1997; Sasaki 1998), evolution of hermaphroditism might have possibly occurred
and Lepetodrilidae and Clypeosectidae constitute a clade within the Lepetelloidea. Ponder & Lindberg (1997) and
(Lepetodriloidea sensu Warén & Bouchet 2001) as revealed in Bouchet et al. (2005) propose fundamentally different
the present phylogeny. phylogenetic hypotheses that regard the gonochoristic
On the other hand, Fretter (1988) described a different Choristellidae with coiled shells as the first offshoot of the
kind of male copulatory structure for another lepetodrilid group. These hypotheses suggest independent evolution of
genus Gorgoleptis McLean, 1988, also from hydrothermal lepetelloid seminal receptacles.
vents (Table 3). The presumed penis of Gorgoleptis is unlike The anatomical features of Seguenziidae have not yet been
that of any known prosobranch in origin and structure, described as thoroughly as the above two groups, but the
because it arises from the left side of the snout, has no connection presence of the penis in males and seminal receptacle in
with the genital opening and must instead function as a females has been confirmed (Quinn 1983, 1991; Haszprunar
pipette (Fretter 1988: fig. 16c). She argued that this penis 1988; Sasaki 1998). The seguenziid penis is a very long verge
evolved independently from that of Lepetodrilus as a result for with a ciliated seminal groove, located posterior to the right
the need for semi-internal fertilization in a deep-sea vent cephalic tentacle and innervated from the cerebral ganglion
habitat (see below), while a seminal receptacle has not been (Quinn 1983, 1991; Hickman 1998). The seminal receptacle
found in Gorgoleptis. Although the multiple origins of the of Seguenzia discovered by Sasaki (1998) is a round pouch in
penes seem to be unequivocal, the understanding of evolution the posterior pallial wall on the left side. The oviduct distally
of the copulatory structure and sperm storage in Lepeto- opens at the right side of the pallial cavity (in Carenzia
driloidea requires more detailed phylogenetic reconstruction carinata; Haszprunar 1988: fig. 2Q) so that fertilization in
and anatomical investigation. The clypeosectid Pseudorimula seguenziids perhaps takes place semi-internally as in the case
apparently lacks both penis and sperm receptacle (Haszprunar of other vetigastropods with copulatory organs. Sasaki (1998)
1988). showed a SEM figure of simple sperm with long and slender
Another striking example of semi-internal fertilization heads in the female receptacle (fig. 67E). Such long-headed
(or ent-aquatic fertilization after Hodgson et al. 1997) occurs euspermatozoa are typically found in semi-internally fertilizing
within the Lepetelloidea, a superfamily associated with aquatic animals (e.g. Healy 1990; Scott & Kenny 1998).
various organic substrates in the deep sea, including sunken Seguenziids occur on mud bottom mainly in bathyal and
wood, fish and whale bones, shark egg cases, cephalopod abyssal depths.
beaks, empty tubes of polychaetes and dead carapaces of Within the superfamily Seguenzioidea, a male organ with
crabs, and also associated with hydrothermal vents and cold a possibly different origin has been described by Warén &
seeps (Haszprunar 1998). Sperm transfer occurs via the Bouchet (1989) for Bathymargarites symplector. This eucycline
modified right cephalic tentacle with a seminal groove in at species from hydrothermal vent sites on the Eastern Pacific
least seven out of eight lepetelloid families (Haszprunar & Rise shows conspicuous sexual dimorphism in the size and
McLean 1996; Haszprunar 1998; Warén & Bouchet 2001). shape of one of the ‘right subocular peduncles.’ The posterior
Of these, Addisoniidae and Choristellidae additionally bear peduncle is hypertrophied in males of Bathymargarites to play
the seminal receptacle at the left side of inner pallial wall, a role as a copulatory organ (Warén & Bouchet 1989:
with no apparent connection with the oviduct (Haszprunar figs 104–107). It is a large and complicated structure with a
1992). The two families may constitute a clade with several, lateral seminal groove and a glandular pad near its distal end,
supposed synapomorphies including shark-egg feeding and appears very different from the penis illustrated for
(Haszprunar & McLean 1996), and therefore each seminal Seguenzia, which is much more slender and situated far back
receptacle and male copulatory organ may have evolved from the cephalic tentacle and ‘subocular peduncle’ (Quinn
only once in the superfamily. Addisonia Dall, 1882 produces 1983: fig. 33). However, the homology or analogy of these
‘ent-aquasperm’ similar to those found in Lepetodrilus (Hodgson male organs can be explicitly discussed only if detailed
et al. 1997), suggesting that semi-internal fertilization occurs anatomical description is available for the two groups, given
in the mantle cavity. their close phylogenetic relationship (Kano & Warén, in
Modification in reproductive strategy to cope with the preparation). The presence or absence of a seminal receptacle
unusual deep-sea habitats of lepetelloids also includes the is unknown in females of Bathymargarites.
evolution of hermaphroditism from separate sexes, the ancestral As mentioned above, eucycline seguenzioids consistently
state in Gastropoda (Ponder & Lindberg 1997). All lepetelloids bear a subocular peduncle with a ciliated lateral groove
except choristellids are simultaneous hermaphrodites immediately posterior to the right eye in both males and
(Haszprunar 1998). The gonochorism in Choristellidae, a females (Fig. 4: sp2). It had been considered a degraded penis
in Calliotropis (e.g. Dall 1889; see Hickman 1992), but all suggests internal (or perhaps semi-internal) fertilization
eucyclines except Bathymargarites seem to make use of external for Zalipais. These euspermatozoa can be classified into
fertilization. Okutani (1994: 126) showed a photograph of ‘introsperm’, in having an extremely long head and a tubular,
live Granata lyrata releasing white fluid, possibly spermatozoa, helically coiled nucleus; such characteristics are typically
from the posterior right side of the mantle cavity. Sperm found in internally fertilizing invertebrates (Healy 1990;
ultrastructure also suggests external fertilization for those Hodgson & Foster 1992). Similar euspermatozoa were
eucycline seguenzioids. The spermatozoa of Calliotropis glyptus reported for two other ‘skeneids’, Microcarina surgerea and
can be classified into the primitive ‘ect-aquasperm’, in having Liotella parvirota (Healy 1990). However, all Zalipais, Microcarina
an extremely short, round head; such a short head is probably Laseron, 1954 and Liotella Iredale, 1915 (a probable synonym
associated with motility demands in scarcely populated deep-sea of Zalipais) may belong to Seguenzioidea, as they show
waters (Healy 1989). The function for the peduncle and its resemblances to seguenzioid skeneimorphs in shell and
ciliated groove is therefore totally unknown in those eucycline radular morphology (A. Warén, personal communication).
seguenzioids, but they might be possibly used for broadcasting Their (semi-) internal fertilization seems to be unrelated
gametes (see Hickman 1992: 252). to that of the true Skeneidae mentioned above, and those
Reproductive biology and anatomy are even less thoroughly ‘introsperm’ might be possibly homologous with the long-
documented for the minute species of Skeneidae, but (semi-) headed euspermatozoa of Seguenziidae.
internal fertilization has been suggested for more than one The least well-known example of (semi-) internal fertilization
lineage within this polyphyletic group. Warén found that a occurs in Pendromidae, one of the rarest vetigastropod
number of skeneids, including the genera Skenea, Skeneoides families. Pendromids are minute snails with skeneimorph
Warén, 1992; Dikoleps Höisaeter, 1968, Lissospira Bush, 1897, shells and without a radula, mainly inhabiting bathyal depths
Protolira Warén & Bouchet, 1993 and Pseudorbis Monterosato, (Warén 1991; Hickman 1998). Female pendromids have a
1884, bear a large appendage with a varying shape on the large seminal receptacle in the posterior left part of the pallial
anterior right corner of the foot (Warén 1991, 1992, 1993: cavity (Warén 1991), while a penis has not been described for
fig. 9; Warén & Bouchet 1993: figs 20D and 21E; A. Warén, males.
personal communication). This presumed penis was present The distant phylogenetic relationships among these clades
in all adult specimens examined, and histological examination and morphological and topological dissimilarities of their
confirmed those skeneids to be simultaneous hermaphrodites penes and seminal receptacles suggest that mating behaviour
(Warén 1993). He argues that its presence may be used as a has occurred at least six independent times in Vetigastropoda.
synapomorphy in grouping the family Skeneidae in a strict As shown in the Table 3, the copulatory and sperm-storage
sense (e.g. Warén & Bouchet 1993). On the other hand, the organs, as well as hermaphroditism, are limited to essentially
subocular peduncle below the right eye (see Fig. 4A: sp1) is deep-sea clades in Vetigastropoda, with the exception of
often hypertrophied to form a very long and laterally ciliated skeneids that often inhabit intertidal and sublittoral waters.
projection in skeneids, and this projection has also been Internal or semi-internal fertilization and hermaphroditism
called a penis (Fretter & Graham 1977; Hickman & McLean are considered to be particularly advantageous for benthic
1990: 96A). However, like the propodial appendage, its function invertebrates in the deep-sea environments (Gage & Tyler
has not been rigorously investigated (Hickman 1992; Warén 1991; Tyler & Young 1999). Most deep-sea invertebrates are
& Bouchet 1993). predicted to reproduce throughout the year, as the seasonally
Sperm morphology provides a more explicit indication of varying temperature that determines reproductive periodicity
mating in skeneimorph species. Healy (1990) reported the in shallow water species is absent in bathyal and abyssal
presence of dimorphic sperm (both fertile euspermatozoa depths (Tyler & Young 1992). Indeed, year-round reproduction
and infertile, multiflagellate paraspermatozoa) in two intertidal has been confirmed in both of the two deep-sea vetigastropods
species of Zalipais Iredale, 1915, while he did not find a penis studied, Calliotropis ottoi and Lepetodrilus fucensis (Colman &
in those ‘skeneids.’ Sperm dimorphism in Gastropoda is limited Tyler 1988; Kelly & Metaxas 2007). Sperm storage is an ideal
to taxa with internal fertilization, irrespective of whether or strategy in such an environment with limited periodic
not a penis or spermatophore is involved in sperm transfer cues for gametogenesis (Hilário et al. 2005). Moreover, low
(Healy 1990; Hodgson & Foster 1992). The proposed functions numerical density of deep-sea organisms makes locating a
of paraspermatozoa include (i) nutrition for euspermatozoa, mate difficult hence sperm storage and hermaphroditism are
principally by lysis of their cell body in the female genital beneficial (Gage & Tyler 1991).
tract with liberation of polysaccharide substances; and (ii) On the other hand, recent investigations have revealed that
transport of the typical euspermatozoa, particularly in species sperm storage is especially common in hydrothermal-vent
without specialized copulatory organs (Giusti & Selmi 1982). invertebrates, including scale worms and tubeworms (Tyler
The morphology of the uniflagellate euspermatozoa also & Young 1999; Hilário et al. 2005). Analogous penes have
been evolved in three vent-endemic lineages within the grants from the Ministry of Education, Science, Sports
Vetigastropoda (Table 3). Sperm storage could prevent the and Culture, Japan (nos. 18770066, 18253007, 15403014 and
rapid dilution of gametes in the turbulent flow regime of 12NP0201).
vents (Tyler & Young 1999). Internal fertilization may also
protect gametes from the high temperature, acidic hydrothermal References
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family Seguenziidae and its taxonomic significance. Biomineralisation,
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in maximum dimension. As body size becomes small, so does (2003). Molecular phylogenetic studies of Gastropoda based on six
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Kano Y. Vetigastropod Phylogeny (2008)

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Vetigastropod phylogeny and a new concept of Seguenzioidea:

Blackwell Publishing Ltd

independent evolution of copulatory organs in the

Introduction to collect because of the minute sizes, rareness or inaccessibility

Species COI H3 18S Locality, depth and habitat

Species COI H3 18S Locality, depth and habitat

Table 2 Nucleotide sequences of primers

*Modified from Colgan et al. (2000).

Fig. 2 Bayesian phylogeny of vetigastropod

Seguenziidae: truly monophyletic?

which is sister to the moderately supported (PP = 94%) clade

Sublittoral to hadal (mainly bathyal)e–g

Abyssal; hydrothermal ventb

Abyssal; hydrothermal ventb

Depth range and habitat

Multiple origins of copulatory and sperm-storage organs in

Left side of inner pallial wall (if present)f,g

Right side of inner pallial walld

Left side of inner pallial walld

Left side of inner pallial walll

their adaptive signiﬁcances. Available knowledge of sperm

also provided for taxa with possible copulatory behaviour.

a relatively well-documented example, both in morphological

Right neck lobeh

and histology of ﬁve species of Lepetodrilus in great detail,

right cephalic tentacle with an open seminal groove. The

female has a seminal receptacle at the right side of the inner

& Metaxas 2007). She found no direct connection between

the receptacle and oviduct, and therefore argued that mature

investigation of sperm morphology supports this argument.

Lepetodrilus produces ‘ent-aquasperm’, which are initially

found in another vent limpet genus Clypeosectus (Haszprunar

1989) are apparently homologous to those of Lepetodrilus in

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