Zoomorphology

, Volume 129, Issue 2, pp 81–91

Homology and morphology of the neogastropod valve of Leiblein (Gastropoda: Caenogastropoda)

Authors

    • Australian Museum
  • Winston F. Ponder
    • Australian Museum
Original Paper

DOI: 10.1007/s00435-009-0101-0

Cite this article as:
Golding, R.E. & Ponder, W.F. Zoomorphology (2010) 129: 81. doi:10.1007/s00435-009-0101-0

Abstract

The valve of Leiblein is a morphological synapomorphy defining Neogastropoda, but is also a significant adaptation in the evolution of carnivorous, predatory feeding and homologues have not been recognised amongst non-neogastropods to date. This study uses histology to examine the valve of Leiblein and associated oesophageal features of a buccinoidean (Euplica scripta—Columbellidae) and two muricoideans (Morula marginalba—Muricidae, and Columbarium pagodoides—Turbinellidae), and comparisons are made with the oesophagus of four non-neogastropods; the tonnoidean out-group Cabestana spengleri and three other littorinimorph caenogastropods. Several morphological details conflict with earlier descriptions of different neogastropod species, such as the presence of a diverticulum in the muricoidean valve and torsion in the buccinoidean valve. This supports recent findings that the valve of Leiblein is morphologically heterogeneous, but, unlike some other studies, does not dispute the homology of the valve in different neogastropod groups. Structure and histology support the homology of the valve of Leiblein in Muricoidea and Buccinoidea and its derivation from elements of the anterior oesophagus of higher littorinimorph caenogastropods (Tonnoidea). A thick, secretory, pseudostratified epithelium lining the ventral anterior oesophagus of C. spengleri is comparable with the tissue lining the glandular chamber of the valve of Leiblein. A modified theory regarding the evolutionary origin of the valve of Leiblein is proposed in which it is homologous to the anterior oesophagus of Tonnoidea.

Keywords

CarnivoryOesophagusTonnoideaBuccinoideaMuricoideaForegut

Introduction

The evolution of carnivory in Caenogastropoda is associated with a variety of morphological and physiological specialisations which facilitate prey detection, capture and digestion. These modifications include increased mobility, enhanced chemosensory abilities (enlarged osphradium), simplification of the midgut and the production of novel digestive enzymes through elaboration of components of the alimentary system, such as the oesophageal gland and salivary glands (Taylor et al. 1980; Taylor 1998; Andrews et al. 1999; Strong 2003). Although several groups of caenogastropods are carnivorous, the largest radiation has occurred within Neogastropoda, a hyper-diverse clade of predatory snails including cones, whelks and drills (Ponder 1974; Taylor et al. 1980; Kantor 1996, 2002). A morphological feature which distinguishes most neogastropods from other carnivorous caenogastropods is the valve of Leiblein; a structure which promotes the unidirectional passage of food through the oesophagus (Amaudrut 1898; Graham 1941; Fretter and Graham 1994).

The valve of Leiblein consists of a short, circular fold of tissue projecting posteriorly into an expanded cavity lined with a thick secretory epithelium (Graham 1941; Andrews and Thorogood 2005; Kantor and Fedosov 2009). Food passing through the circular fold into the cavity is coated with lubricating mucous secretions while strong, posteriorly directed ciliary currents around the apex of the fold prevent anterior regression of particles (Graham 1941). The hypothesised function of the valve may be to prevent regurgitation of food during feeding (Graham 1941), retain digestive secretions from the gland of Leiblein (Ponder 1974) or separate liquid from solid food for transport to the gland of Leiblein (Andrews and Thorogood 2005). Andrews and Thorogood (2005) described the detailed anatomy of the valve and gland of Leiblein of the muricid Nucella lapillus (Linnaeus, 1758). They discovered that a ‘siphon’ (=ventral groove or ‘scar’ dividing the oesophageal epithelium), bordered by the swollen dorsal folds, runs from the valve to the aperture of the gland of Leiblein and may be involved in the transportation of liquid and solutes to the absorptive gland of Leiblein (Andrews and Thorogood 2005).

The valve of Leiblein occurs in all major groups of neogastropods, although in several groups it is greatly reduced or lost (Ponder 1974; Taylor and Morris 1988; Kantor 2002; Andrews and Thorogood 2005). Until a similar structure was recently identified in two species of Conidae (Kantor and Taylor 2002), the valve of Leiblein was not known from Conoidea. No homologue to the valve of Leiblein has been identified in the alimentary system of other caenogastropods. The unique structure and limited occurrence of the valve of Leiblein have resulted in it being considered one of the main synapomorphies of Neogastropoda (e.g., Taylor and Morris 1988), but its detailed structure has been examined in few taxa (Graham 1941; Kantor and Taylor 2002; Andrews and Thorogood 2005). The recent study by Kantor and Fedosov (2009) provided a wealth of morphological information, examining the valve of Leiblein in seven neogastropods from all major lineages.

Two main theories have been proposed to explain the evolution and anatomical homology of the valve of Leiblein.
  1. 1.

    Graham (1941) postulated that the valve of Leiblein is derived from the dorsal food channel of the mid-oesophagus. He proposed that the ventral section (oesophageal gland) of the mid-oesophagus (including the section in the vicinity of the valve of Leiblein) was stripped from the dorsal section to form the gland of Leiblein, allowing the remaining dorsal section of the oesophagus to be ‘pulled’ through the nerve ring. He postulated that the dorsal food channel of the mid-oesophagus, including the dorsal folds, was modified to form the valve and its glandular chamber. Evidence for this theory includes the presence of a ‘scar’ on the morphologically ventral surface of the valve of Leiblein, indicating the site of separation from the oesophageal gland, and the ‘lubricating’ secretions of the tissue lining the valve which Graham identified with the epithelia lining the dorsal food channel. Graham’s theory was further illustrated by Andrews and Thorogood (2005), who agreed that the valve of Leiblein was a modification of the dorsal section of the mid-oesophagus.

     
  2. 2.

    Ponder (1974) postulated that neogastropods are derived from ‘archaeogastropod’ or ‘lower caenogastropod’ stock, rather than higher caenogastropods and that the valve of Leiblein is a modification of ‘archaeogastropod’ oesophageal (buccal) pouches. These structures are glandular diverticula which lie immediately posterior to the buccal mass. However, this theory of the derivation of neogastropods is not supported by recent phylogenetic analyses which indicate that higher littorinimorph caenogastropods are the sister to neogastropods (Healy 1988; Ponder and Lindberg 1997; Riedel 2000; Strong 2003; Ponder et al. 2008). Ponder (1974) also suggested that the anterior oesophagus of neogastropods was an elongation of the posterior buccal cavity.

     

These hypotheses are incompatible, but there is limited evidence available to support either case. Perhaps due to the paucity of information, both Graham (1941) and Kantor and Fedosov (2009) concluded that the valve of Leiblein of Muricoidea and that of Buccinoidea are not homologous. However, the discussion is incomplete without comparing the homology of the tissues composing the valve of Leiblein to the oesophagus of other caenogastropods.

In order to address the questions raised earlier, we investigated the oesophagus of representative taxa from two neogastropod superfamilies, Muricoidea and Buccinoidea, a ranellid (Tonnoidea) and three other littorinimorph caenogastropods, to investigate the derivation and homology of the valve of Leiblein.

Materials and methods

Specimens of the neogastropods Euplica scripta (Lamarck, 1822) (Columbellidae, Buccinoidea) and Morula marginalba (Blainville, 1832) (Muricidae, Muricoidea) and the other caenogastropods Cabestana spengleri (Perry, 1811) (Ranellidae, Tonnoidea), Strombus gibberulus (Linnaeus, 1758) (Strombidae, Stromboidea) and Conuber melastomum (Swainson, 1822) (Naticidae, Naticoidea) were collected alive near Sydney, New South Wales or Heron Island, Queensland (Table 1) and relaxed in equal volumes of filtered sea water and 7.5% MgCl2 prior to fixation in Bouin’s fluid for 24 h and preservation in 70% EtOH. Specimens of Lamellaria sp. (Velutinoidea, Velutinidae) and the neogastropod Columbarium pagodoides (Watson, 1882) (Turbinellidae, Muricoidea) were examined from the Australian Museum collections.
Table 1

Caenogastropod specimens examined in this study with classification to superfamily, family and species with authority

Superfamily

Family

Species

Locality

Date

Collector

Voucher

Stromboidea

Strombidae

Strombus gibberulus (Linnaeus, 1758)

Shark Bay, Heron Island, QLD

23/08/2005

M. Kosnik

C212924

Naticoidea

Naticidae

Conuber melastomum (Swainson, 1822)

Careel Bay, Pittwater, NSW

2/10/2005

R. Golding and M. Hill

C212913

Velutinoidea

Velutinidae

Lamellaria sp.

E of Yamba, NSW, dredged at 70 m

21/04/1996

K. J. Graham, FRV Kapala

C405364

Tonnoidea

Ranellidae

Cabestana spengleri (Perry, 1811)

Mona Vale Beach, Sydney, NSW

23/06/2005

R. Golding and P. Golding

C212922

Buccinoidea

Columbellidae

Euplica scripta (Lamarck, 1822)

Bradley’s Head, Port Jackson, NSW

2/01/2006

R. Golding, W. F. Ponder and D. Beechey

C212899

Muricoidea

Muricidae

Morula marginalba (Blainville, 1832)

Mona Vale Beach, Sydney, NSW

1/02/2007

R. Golding and P. Golding

C212911

Muricoidea

Turbinellidae

Columbarium pagodoides (Watson, 1882)

Dredged off Sydney, NSW

7/12/1972

FRV Kapala

C089674

Specimen collection details including locality, date, collector and Australian Museum voucher numbers are also given

The head and anterior alimentary system of one individual from each species was removed by dissection then dehydrated and saturated with Paraplast™ paraffin, using a Tissue-Tek® VIP processor. The specimens were then embedded in paraffin using a Tissue-Tek® TEC embedding station and serially sectioned on an American Optical microtome at between 5 and 7 μm, depending on specimen size. The sections were stained with Mayer’s Haematoxylin and Cason’s trichrome (acid fuchsin, aniline blue and orange G) and photographed using an Olympus DP70 digital camera mounted on an Olympus BX50 microscope with Olympus DPController image acquisition software. Additional specimens of C. spengleri were dissected under a Leica dissecting microscope with a camera lucida attached, to assist illustration of the oesophageal folds.

Results

Littorinimorph caenogastropods

The anterior oesophagus of the herbivore Strombus gibberulus (Strombidae), drilling carnivore Conuber melastomum (Naticidae) and grazing carnivore Lamellaria sp. (Velutinidae) differs mainly in the degree to which the dorsal folds are developed (Fig. 1). Two dorsal folds are present, marking the lower boundary of the dorsal food channel. The dorsal folds in the anterior and mid-oesophagus of Lamellaria sp. are asymmetrical, with the left dorsal fold (ldf) several times longer than the right (rdf) (Fig. 1b). A short section of ventral fold is present in the anterior oesophagus of S. gibberulus (data not shown). The low epithelium lining the anterior oesophagus is uniformly composed of narrow columnar cells with basal nuclei and dark purple-stained cell contents, interspersed with mucous cells. The dorsal food channel is more densely ciliated than the ventral food channel in C. melastomum and S. gibberulus (Fig. 1a, c). Posteriorly, the ventral channel in the mid-oesophagus expands substantially to form a septate oesophageal gland lined with distinct, protein-secreting, glandular cells which are not found elsewhere in the oesophagus.
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Fig. 1

Transverse histological sections through the oesophagus of three non-neogastropod taxa. Sections are taken from the anterior oesophagus, posterior to the buccal mass but anterior to the oesophageal gland and stomach. aConuber melastomum (Naticidae, Naticoidea). bLamellaria sp. (Velutinidae, Velutinoidea). cStrombus gibberulus (Strombidae, Stromboidea). cn circumoesophageal nerve ring, dfc dorsal food channel, ldf left dorsal fold, ow oesophageal wall, rdf right dorsal fold, sd salivary gland duct

In the tonnoidean Cabestana spengleri, the anterior oesophagus in the region of the buccal ganglia is dominated by a pair of broad, elongate, symmetrical dorsal folds (Fig. 2a; ldf, rdf) and a much smaller pair of ventrolateral folds (vlf) situated laterally on the inner oesophageal wall. The ventrolateral folds do not continue posteriorly, but the dorsal folds continue through the anterior and mid-oesophagus, with the left dorsal fold superior to and approximately twice the length of the right dorsal fold (Fig. 2b–d). When examined by dissection, the anterior oesophagus (leading to the oesophageal gland) is effectively divided into two separate channels; a dorsal food channel and a ventral glandular channel, separated by a double layer of overlapping dorsal folds (Fig. 2e).
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Fig. 2

Cabestana spengleri (Ranellidae, Tonnoidea). Transverse histological sections through the oesophagus at the level of the buccal ganglia (a), through the anterior oesophagus (b, c) and mid-oesophagus with oesophageal gland (d). e Oesophagus of C. spengleri dissected dorsally (anterior at top of image) with left dorsal fold displaced outwards to reveal the ventral glandular pad. Stippling indicates the presence of glandular epithelium on the ventral surfaces of the dorsal folds (visible by transparency on the right dorsal fold). bg buccal ganglion, dfc dorsal food channel, ldf left dorsal fold, og oesophageal gland, pse pseudostratified epithelium, rdf right dorsal fold, sd salivary gland duct, vgp ventral glandular pad, vlf ventrolateral fold

The dorsal food channel of the anterior oesophagus, bordered ventrally by the dorsal folds, is lined with a relatively low, densely ciliated, columnar epithelium composed of basophilic (dark purple-stained) cells with centrally positioned nuclei, interspersed with occasional mucous cells (Fig. 2a, b). The ventral channel is entirely covered with a much taller, pseudostratified epithelium (Fig. 2b; pse) composed of glandular cells which stain pale purple with Cason’s trichrome and contain basal nuclei. Small, wedge-shaped ciliary cells are positioned between the glandular cells, forming a second layer of nuclei near the surface. The epithelium lining the ventral channel is divided into three discrete sheets; two covering the ventral surfaces of the dorsal folds and a thick median sheet referred to here as the ventral glandular pad (Fig. 2b; vgp). The cells composing the glandular epithelium on the ventral surfaces of the dorsal folds show some histological variation, as the cell contents become progressively more transparent and the cells more inflated with cell contents posteriorly (Fig. 2c).

Posterior to the circumoesophageal nerve ring, the ventral glandular epithelium is reduced in height and confluent with the oesophageal gland (Fig. 2d; og). The oesophageal gland originates as a series of septate outpockets from the ventral wall of the mid-oesophagus, and these pockets are lined with a distinct epithelium composed of bright red-stained, protein-secreting cells (Fig. 2d). The dorsal folds adjacent to the oesophageal gland retain their asymmetry and a low epithelium typical of the anterior oesophagus.

Neogastropoda

Morula marginalba (Muricidae) and Columbarium pagodoides (Turbinellidae) both have a valve of Leiblein situated immediately anterior to the cerebral ganglia. The interior surface of the anterior oesophagus is simple apart from a pair of broad, low dorsal folds (Fig. 3a; ldf, rdf) situated laterally above the salivary gland ducts (sd). The anterior junction of the valve is marked by the development of an incomplete circular fold (Fig. 3b, e, f; cf). The walls of the circular fold form a cone-shaped tube, directed posteriorly, which is divided by a ventral slit (Fig. 3b, c) (described in the muricid Nucella lapillus by Graham 1941). The oesophageal wall around the circular fold is expanded to form a thick-walled, glandular chamber. The anatomically ventral surface of the glandular chamber is marked by a non-glandular strip of oesophageal wall (the ventral groove, Fig. 3g; vg) bordered by the dorsal folds (left larger than right) extending from the oesophageal wall, which are particularly evident in C. pagodoides (Fig. 3g). The ventral groove spirals from an anterior ventral position towards the right wall of the valve, due to torsion. At the junction of the circular fold with the oesophageal wall, the ventral slit in the circular fold is confluent with the ventral groove in the pseudostratified epithelium lining the glandular chamber (Fig. 3c, d, g, h).
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Fig. 3

Transverse histological sections through the valve of Leiblein of the muricoideans Morula marginalba (Muricidae) (ad) and Columbarium pagodoides (Turbinellidae) (eh). a Oesophagus anterior to valve. b, e, f Anterior margin of valve, with circular fold and glandular chamber lined with mucous pad. c, g Mid valve with enlarged glandular chamber containing ciliated circular fold. d, h Posterior valve with narrow lumen. cf circular fold, div diverticulum, ldf left dorsal fold, mp mucous pad, pse pseudostratified epithelium, rdf right dorsal fold, sd salivary gland duct, vg ventral groove

The dorsal and ventral channels of the anterior oesophagus, and the interior surface of the circular fold, are lined with a relatively low epithelium containing mucous cells (Fig. 3a, e). Extremely long cilia are present on the interior surface of the circular fold, particularly around the posterior margin (Fig. 3c, g). The anterior dorsal and ventral surfaces of the glandular chamber and the outer surface of the circular fold are dominated by mucous cells (the mucous pad, Fig. 3b, f; mp). The remainder of the glandular epithelium within the chamber is composed of a pseudostratified epithelium (Fig. 3c, d; pse) of very tall, pale to dark purple-stained cells with basal nuclei, interspersed with sparsely ciliated cells to create an apparent double layer of nuclei (Fig. 3c, d, f–h). The posterior of the chamber is narrower, and the glandular epithelium tapers off to be replaced by low columnar cells similar to those found in the anterior oesophagus (Fig. 3h).

A small diverticulum (Fig. 4; div) from the glandular chamber is present at the posterior of the valve. The diverticulum is located beneath the pseudostratified epithelium of the right dorsal fold (Fig. 4a, d), opening posteriorly to the right of the ventral groove and burrowing beneath the epithelium as a blind-ending passage which is rear facing. The aperture of the diverticulum is positioned very close to the ventral groove, but its path beneath the epithelium diverges from the ventral groove. The diverticulum is bottle-shaped in cross section in C. pagodoides (Fig. 4f) but much smaller and roughly circular in cross section in M. marginalba (Fig. 4b, c). The diverticulum is lined with a low, cuboidal, unciliated epithelium (Fig. 4c, f).
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Fig. 4

Transverse histological sections through the valve of Leiblein of the muricoideans Morula marginalba (Muricidae) (ac) and Columbarium pagodoides (Turbinellidae) (df). a, d Middle region of valve showing blind-ending diverticulum. b, e Posterior region of valve showing diverticulum. c, f Detail of diverticulum at broadest point. cf circular fold, div diverticulum, pse pseudostratified epithelium, vg ventral groove

The anterior oesophagus of Euplica scripta (Columbellidae) has low dorsal folds on the lateral walls, but these are not visible as the anterior oesophagus approaches the valve of Leiblein (Fig. 5a). A valve of Leiblein is present anterior to the circumoesophageal nerve ring, and unlike the descriptions of the oesophagus of Buccinum undatum Linnaeus, 1758 given by Graham (1941) and Kantor and Fedosov (2009), is twisted by torsion. Within the valve of Leiblein, the circular fold of tissue forms a complete cone which lacks the ventral slit of the muricoidean taxa examined (Fig. 5b–d). The epithelium lining the glandular chamber is marked by two ventrolateral longitudinal grooves (Fig. 5c, d; arrowheads) which are equidistant from the midline and spiral around the valve towards the right.
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Fig. 5

Transverse histological sections through the valve of Leiblein of a buccinoidean, Euplica scripta (Columbellidae), ordered from anterior to posterior. a Oesophagus anterior to valve. b Anterior valve with circular fold fused to mucous pad. c Mid valve with ventrolateral grooves (arrowheads). d Posterior valve with thickened glandular epithelium. cf circular fold, gp glandular pad, mp mucous pad, oe oesophagus, pse pseudostratified epithelium, sd salivary gland ducts

The epithelium lining the anterior oesophagus is composed of low, columnar cells with centrally positioned nuclei and sparse ciliation. The interior of the circular fold has a similar histology, but has longer and denser cilia (Fig. 5c). A ciliated, mucous epithelium is restricted to the dorsal wall of the glandular chamber, surrounding the fused surface of the circular fold (Fig. 5b, c). The remainder of the glandular chamber is composed of a tall, psueodostratified epithelium (Fig. 5b–d; pse) of pale purple-stained cells with basal nuclei, overlayed by a layer of densely ciliated cells.

Discussion

Inadequate knowledge of the morphology of the valve of Leiblein has impeded interpretation of the functional and evolutionary significance of this structure. This study has described the morphology and histology of the anterior oesophagus for a small sample of neogastropods and non-neogastropod out-groups. The results have shown additional anatomical details of the valve of Leiblein in three neogastropod species and support for the homology of this structure within Neogastropoda. This study has also demonstrated similarities between the tissues present in the anterior oesophagus of a putative out-group to Neogastropoda, leading to a new hypothesis on the evolution of the valve of Leiblein.

Morphological variation of the valve of Leiblein

Previous studies have demonstrated the morphological heterogeneity of the valve of Leiblein across different neogastropod groups (Graham 1941; Kantor and Fedosov 2009). There are several inconsistencies between previous descriptions of the valve of Leiblein of Buccinoidea and Muricoidea and those presented here, which may be due to either more detailed examination or to differences between species. The valve of Euplica scripta (Buccinoidea) was found to be twisted by torsion, unlike the buccinoidean valves described by Graham (1941) and Kantor and Fedosov (2009). In addition, the blind-ending diverticulum detected in the right ventrolateral surface of the glandular chamber of the muricoidean valve has not been described in previous studies. This curious structure has no obvious function but is perhaps related to the operation of the siphon (i.e., the ventral groove) which connects the valve to the gland of Leiblein in Nucella sp. (Andrews and Thorogood 2005).

Morphological variation in the structure of the valve of Leiblein has been interpreted by some authors as evidence of independent derivation (Graham 1941; Kantor and Fedosov 2009), in opposition to the more widely held view that the valve of Leiblein is a highly significant morphological synapomorphy supporting the monophyly of Neogastropoda (e.g., Taylor and Morris 1988; Strong 2003). The valve of Leiblein present in some conoidean and cancellarioidean taxa is not well characterised and is of uncertain homology to the valve in Buccinoidea and Muricoidea (Kantor and Fedosov 2009) and, as they were not examined in this study, are not the focus of the following discussion.

Graham (1941) theorised that the buccinoidean and muricoidean valves are not homologous because only the latter are positioned on the site of torsion. Based on the findings of the present study, we dispute this reasoning, because at least one buccinoidean species (E. scripta) displays torsion through the valve of Leiblein. Kantor and Fedosov (2009) also consider buccinoidean and muricoidean valves to be putatively analogous, in part because the ventral groove between the dorsal folds which is present in Muricoidea does not extend through the glandular chamber of the buccinoidean valve. However, Graham (1941) illustrated the valve of Leiblein of Buccinum undatum (Buccinidae) with a ventral groove originating in the posterior part of the glandular chamber of the valve, which he interpreted as the remainder of the dorsal folds. The buccinoidean examined in this study does not have a ventral groove, but the glandular chamber is clearly marked by a pair of ventrolateral depressions which may be the vestigial remains of the tissue separating the dorsal folds from the oesophageal wall. This feature requires further examination of other taxa to determine its significance.

The homology of the valve of Leiblein of Buccinoidea and Muricoidea is supported by the following similarities:
  1. 1.

    The gross structure of each valve is similar, with a narrow anterior aperture leading to a posteriorly directed circular fold, surrounded by a glandular chamber.

     
  2. 2.

    The valve is positioned immediately anterior to the nerve ring.

     
  3. 3.

    The epithelium lining the circular fold is relatively low and dark-staining.

     
  4. 4.

    The glandular epithelium is predominantly pseudostratified, with dense ciliation.

     
  5. 5.

    The glandular epithelium is differentiated near the junction with the circular fold, where inflated cells with pale-stained contents (probably mucous cells) are present.

     
  6. 6.

    The glandular epithelium is marked ventrally by a longitudinal groove (Muricoidea) or pair of indentations (Buccinoidea).

     

These similarities strongly support the homology of the valve of Leiblein. The homology of this structure with non-neogastropods is discussed in the following paragraphs.

Evolutionary derivation of the neogastropod valve of Leiblein

The evolutionary origin of the valve has not been investigated in any recent comparative morphological studies, nor are there any previous reports of valve of Leiblein-like structures in the oesophagus of any non-neogastropod taxa. This study presents evidence of a putatively homologous structure in the anterior oesophagus of the ranellid, Cabestana spengleri.

There is considerable evidence that the circular fold in the valve of Leiblein is a modification of (and homologous to) the dorsal folds, as proposed by Graham (1941) and supported by Andrews and Thorogood (2005). In Muricoidea, the circular fold is divided ventrally, and the base of each side of the circular fold is fused to the corresponding dorsal fold (Fig. 3b). The presence of the dorsal folds through the glandular chamber is also confirmed by the fact that the left fold is larger than the right. This asymmetry is also present on the anterior and mid-oesophageal dorsal folds of C. spengleri (Fig. 2b), Lamellaria sp. (Fig. 1b) and some other caenogastropods (Andrews and Thorogood 2005). Further evidence is provided by histology, with both the dorsal food channel (bordered by the dorsal folds) and the circular fold lined with a relatively low, dark-staining, ciliated epithelium.

Histological examination of the anterior oesophagus of C. spengleri shows that a very thick epithelium lining the ventral channel closely resembles the lining of the glandular chamber of the valve of Leiblein. Both tissues have a strikingly similar histology—a thick, pseudostratified epithelium (Brown 1969; Kantor and Fedosov 2009) with tall, columnar cells, bearing low ciliation. In both groups, the epithelium is ventral in the anterior oesophagus, although the glandular chamber of the valve in muricoids is divided by a narrow strip of non-glandular tissue between the dorsal folds. This groove is possibly inconsistent with the homology inferred here (also see in the following paragraphs), but may be a specialisation associated with the siphon (i.e., ventral groove) which connects the valve to the gland of Leiblein. A reduction in the epithelium in this region in some taxa would perhaps be advantageous to the passage of liquid and solutes (Andrews and Thorogood 2005).

As outlined in the Introduction, two opposing theories have been put forward to explain the evolutionary origin of the valve of Leiblein. Graham’s (1941) theory of oesophageal modification proposed that the valve of Leiblein is homologous to the mid-oesophagus of other caenogastropods. He suggested that the ventral tissue of the mid-oesophagus was stripped entirely away from the mid-oesophagus (including the valve) to form the gland of Leiblein, leaving only a ventral groove (‘scar’) in the ventral midline of the oesophagus. The results presented here do not support this interpretation, because the epithelium lining the glandular section of the valve of Leiblein is totally dissimilar to the tissue lining the dorsal section (dorsal food channel) of the mid-oesophagus of other caenogastropods. The alternative theory, put forward by Ponder (1974), has the valve of Leiblein derived from the oesophageal pouches in the posterior region of the buccal mass of an archaeogastropod or lower caenogastropod ancestor. As discussed earlier, this is unlikely given current phylogenetic interpretations of Gastropoda (for example, Ponder and Lindberg 1997; Aktipis et al. 2008).

Instead, we propose a modification of Ponder’s (1974) hypothesis. The histological similarities between the glandular layers in the valve of Leiblein and the anterior oesophagus of the ranellid C. spengleri suggest that the valve is homologous to the anterior oesophagus of closely related caenogastropods. There is good evidence for a close relationship between Tonnoidea and Neogastropoda (Riedel 2000; Colgan et al. 2007; Ponder et al. 2008), supporting the theory that the epithelial layers in these structures are corresponding and homologous.

Figure 6 shows a hypothetical pathway for the evolution of both the valve of Leiblein of Neogastropoda (represented here by a buccinid and a muricid species) and the long anterior oesophagus of C. spengleri from a putative common ancestor with a glandularised ventral layer in a very short anterior oesophagus. The elongation of the anterior oesophagus occurred differently in both groups in response to the necessity for a longer foregut with the development of a proboscis. In Tonnoidea (or close relatives to them), groups such as Pisanianuridae (Waren and Bouchet 1990) have a very short oesophagus and proboscis. In most tonnoideans (including C. spengleri), the anterior oesophagus has simply elongated, but in Neogastropoda, the anterior oesophagus is a new structure derived from the dorsal part of the posterior buccal cavity (Ponder 1974). We propose that the original short glandular anterior oesophagus was carried backwards and further compacted to form the valve of Leiblein.
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Fig. 6

Diagrams of the key components of foregut anatomy in a hypothetical pre-proboscidate common ancestor (a), Cabestana spengleri (b) and a neogastropod such as Morula marginalba, Columbarium pagodoides or Euplica scripta (c). Homology is inferred by shading: dark grey, buccal mass or derived from buccal mass; stippled, anterior oesophagus; light grey, mid-oesophagus. Cross sections at the positions indicated by lines on (b) and (c) through the anterior oesophagus of C. spengleri (d), Euplica scripta (e) and Columbaruim pagodoides (f) show homologous tissue layers in the anterior oesophagus and valve of Leiblein: black, dorsal folds; stippled, pseudostratified, glandular epithelium; hatched, low, non-glandular epithelium. bm buccal mass, dfc dorsal food channel, gL gland of Leiblein, ldf left dorsal fold, mp mucous pad, nr nerve ring, og oesophageal gland, rdf right dorsal fold, vL valve of Leiblein

This theory is supported by the weak or absent dorsal folds of the anterior section of the neogastropod oesophagus. In other caenogastropods, the dorsal folds are prominent in the anterior oesophagus, but they are absent or reduced in the buccal region of the gut (Strong 2003). In addition, evidence for the buccal origin of the anterior part of the oesophagus in neogastropods comes from ontogenetic studies. Previous investigations of the ontogenetic development of the caenogastropod digestive system suggest that part of the foregut of predatory species with planktotrophic larvae is formed prior to metamorphosis from either a ventral outpocketing of the larval buccal mass or, in the most extreme cases, an isolated parallel anterior oesophagus and buccal mass (Ball et al. 1997; Page and Pedersen 1998; Page 2000, 2005). Page (2000, 2005) described the foregut ontogeny of a nassariid and showed that the post-metamorphic buccal mass develops separately from the larval foregut. In addition, the anterior oesophagus forms from an elaboration of this parallel buccal capsule (Page 2005) supporting the buccal origin of that structure.

Acknowledgments

This research was supported by a Chadwick Biodiversity Fellowship from the Australian Museum, Australian Biological Resources Study PhD Research Scholarship, funding from an Australian Museum Postgraduate Award and University of Sydney Postgraduate Research Support Scheme awarded to REG. The constructive comments of three anonymous reviewers greatly improved the manuscript. Professor Maria Byrne of the Department of Anatomy and Histology at the University of Sydney provided guidance and laboratory space and is thanked for her generous support. Alison Miller and Ian Loch at the Australian Museum are thanked for their kind assistance.

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