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New Molluscan larval form: brooding and development in a hydrothermal vent gastropod, Ifremeria nautilei (Provannidae).

Paradoxically, organisms physiologically adapted to the deep sea, including extreme conditions at hydrothermal vents, seldom display life-history modifications unique to these unforgiving environments. Although internal fertilization is more common at vents than in shallow water, developmental modes and larval forms are typically similar in deep-sea animals and their shallow-water relatives (1), (2), (3), (4). Here we report the first documented exception to this general rule in Ifremeria nautilei (Provannidae), a hydro-thermal vent snail living at 1700-2900 m depth in the western Pacific.

The gastropod family Provannidae includes five genera (Provanna, Alviniconcha, Cordesia, Debruyeresia, Ifremeria) and is known from hydrothermal vents, hydrocarbon seeps, and large detrital falls (wood, animal carcasses) in the deep sea. Sperm ultrastructure (5), (6) and molecular data (7) reveal affinities with intertidal periwinkles and their relatives (Littorinoidea) in the Caenogastropoda, the largest of five main gastropod clades, which contains [approximately equal to]60% of living species (8). A large multi-gene molecular data set has revealed that the deep-sea gastropod genus Abyssochrysos (Abyssochrysidae) is nested within the Provannidae (9). Consequently, until a comprehensive revision is completed and family-level relationships refined, we refer to the entire assemblage as the Abyssochrysoidea.

While most abyssochrysoids are small (< 20 mm in adult length) grazers on bacteria and detritus, members of Ifremeria and Alviniconcha host chemoautotrophic sulphur oxidizing symbiotic bacteria that contribute most of the metabolic requirements, allowing them to reach large adult sizes (> 85 mm) (10). Both planktotrophic (feeding) and non-planktotrophic larval development occur among abyssochrysoids, but the spawn and early development are known for only one species, Provanna lomana, which exhibits encapsulated development with adelphophagy (sibling cannibalism). It is not known if the young emerge as veliger larvae or crawling juveniles, but the large, simple, paucispiral protoconch (larval shell) is indicative of non-plank-totrophic development (11), (12). In Ifremeria, Alviniconcha, Cordesia, Debruyersia, and some fossil members of Provanna, the apical whorls of the protoconch (protoconch I) are lacking (i.e., decollate) and the opening is sealed with a calcareous plug. In these forms, protoconch II comprises 1.5-2 whorls and is ornamented with numerous orthocline riblets and fine spiral threads (12), (13). The size difference between the eggs and the decollate larval shells is too large to be explained by lecithotrophy (14), and the presence of elaborate, reinforcing ornamentation is also taken to indicate planktotrophic development (14), (15).

Ifremeria nautilei is unique among abyssochrysoids in possessing a brood pouch in the foot of the female (12) (Fig. 1A-D). Small, ovoid, yolky eggs, [approximately equal to] 40-45 [micro]m in length, are transported from the ovary to the pallial oviduct (Fig. 1E), which lacks the albumen, capsule, and jelly glands responsible for producing and provisioning the egg capsule in oviparous and some ovoviviparous species. Secretions from an unspecialized basophilic epithelium entangle strings of fertilized eggs (Fig. 1G) that are conveyed through a prominent furrow from the mantle cavity to a lateral groove along the sole of the foot. The egg strings enter a central ciliated pore (Fig. 1C-D) on the sole, probably via a deep furrow formed by the foot, as in other gastropods that use the foot to manipulate their spawn, but this process has not been observed. The pore opens to a large brood pouch, roughly circular in cross section, containing thousands of developing embryos. The pouch is surrounded by several layers of circular muscles and is lined with a simple, thin, primarily unciliated, squamous-to-cuboidal epithelium. A variable number of branching septae (Fig. 1B) radiate from the pore toward the rear and side walls, subdividing the interior into a series of chambers. Muscular tissue from the surrounding layers penetrates the septae. A thin, darkly staining noncellular substance of unknown composition, possibly cuticular, lines the interior surfaces of the brood pouch (Fig. 1F).

[FIGURE 1 OMITTED]

The metapodial pedal gland present in all other abyssochrysoids is absent in Ifremeria nautilei, and we hypothesize that it has been co-opted for brooding (12). Brood pouches within the head-foot have evolved independently several times within the unrelated caenogastropod super-family Cerithioidea. However, these penetrate the cephalic hemocoel from a pore on the side of the neck or the foot through modification of an external egg groove. A single non-homologous instance of brooding in a modified anterior pedal gland is known in members of the West African genus Cymbium (Volutidae) (16). The pouch of Ifremeria is the only known instance of brooding in a metapodial pedal gland, and no other vent or deep-sea gastropod is known to brood.

Although the duration of incubation is not known, all embryos in the brood pouch of a single individual are at comparable stages of development. Embryos arrive in the pouch soon after fertilization, followed by formation of a stereoblastula. The mode of gastrulation is not known. The first larval stage differs from the classic gastropod trochophore in lacking a girdle of multiciliated trochoblast cells; instead, it is fully ciliated, with simple cilia extending through pores of an external cuticular layer (Fig. 2A-D, E, G). This cuticle resembles those of some polychaetes, including sipunculan pelagophaeras, that retain the egg envelope into the larval stages (17), (18). Larval cuticles are previously unknown in gastropod larvae, although the pericalymma larvae of protobranch bivalves and neomenioid aplacophorans have cellular tests. Cilia on the posterior end are distinctly longer than the other cilia (Fig. 2B, F) At the time of larval release or soon thereafter, two small anterior lobes of slightly different size become evident (Fig. 2F). Larvae were released from the brood pouch at this stage under laboratory conditions on multiple occasions.

The antero-posterior axis is defined by the position of the mouth (Fig. 2G, I, J). Larvae are neutrally buoyant and swim with the posterior end facing forward (http://www.biolbull.org/supplemental/), with the longer posterior lobe cilia apparently functioning like the anterior apical tuft of a trochophore. The larvae exhibit no phototactic behavior when exposed to unidirectional white light. Although the larva has a stomodeum, the gut is blind and the larva is packed with yolk granules (Fig. 2 E, H), suggesting that it does not feed.

About 15 days after their release from the brood pouch, some of the larvae reared at room temperature metamorphosed into shelled veligers (Fig. 2K, L); larvae reared at 4 [degrees]C developed more slowly and died before metamorphosis. The velum, which develops at the bi-lobed anterior end flanking the mouth, possesses putative simple and compound cilia, but details of shell ornamentation were not yet evident. Neither settlement nor metamorphosis into benthic juveniles was observed.

The newly released stage is a previously unknown larval type that we name "Waren's larva" in honor of Anders Waren (Swedish Museum of Natural History), a prolific gastropod systematist and specialist in deep-sea gastropods who first noted the brood pouch. The trochophore larva (19), veliger larva (20), and echinospira larva (21) of benthic gastropods and the polytrochous larva (22) of pelagic pteropods have all been known since the 19th century. Waren's larva is the first new gastropod larval form to be described in more than 100 years. While the term trochophore has been defined in various ways (23), (24), even the broadest definition cannot be applied to Waren's larva. No other caenogastropod is known to possess a free-swimming pre-veliger larval stage, none is known to possess a cuticle, and no other gastropod larva swims with its posterior end forward. Indeed non-planktonic early development is touted as one of the significant innovations contributing to the evolutionary success of caenogastropods (8). However, the significance of releasing motile pre-veliger larvae is uncertain. Free-swimming pre-veligers have now been confirmed in one oviparous species of Provanna (Waren, pers.comm.), indicating that this larval form is correlated neither with brooding nor with vent habitats. Indeed, the presence of decollate larval shells among planktotrophic members of the family may indicate that this larval form is widespread within the group. If so, it is possible that the enhanced dispersal capacity afforded by this free-swimming stage would convey a significant advantage in the patchy and ephemeral habitats of the deep sea. Longer dispersal times increase the area that a larva can travel before it must settle, and thus the probability that a larva will encounter a suitable habitat patch. Encounter is a necessary precursor to larval detection of, and response to, settlement cues. In any case, development of a novel mode of internal brooding in conjunction with planktonic early development is remarkable and challenges the assumption of similarity in life-history strategies between shallow-water marine species and their deep-water relatives.

Acknowledgments

We are grateful to Anders Waren for bringing the brood pouch to our attention, for providing SEM images of some of the larvae, and for loaning samples from his own collection. We thank Paul Tyler for histological expertise and help with sample processing; OIMB and the Smithsonian Institution for SEM work; and Paul Greenhall, Marilyn Schotte, Gabriela Vega, Kamille Hammerstrom, Svetlana Maslakova, and Maya Wolf for assistance with handling specimens. The work was supported by National Science Foundation (Grants # OCE-0241250 and OCE-0527139), JSPS Research Fellowships for Young Scientists, KAKENHI (18405006), and grants from the ChEss/Fondation Total, Dr. Earl H. Myers and Ethel M. Myers Oceanographic and Marine Biology Trust, and the David and Lucille Packard Foundation.

Literature Cited

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(11.) Waren, A., and W. F. Ponder. 1991. New species, anatomy, and systematic position of the hydrothermal vent and hydrocarbon seep gastropod family Provannidae fam. n. (Caenogastropoda). Zool. Scr. 20: 27-56.

(12.) Kaim, A., R. G. Jenkins, and A. Waren. 2008. Provannid and provannid-like gastropods from the late Cretaceous cold seeps of Hokkaido (Japan) and the fossil record of the Provannidae (Gastropoda, Abyssochrysoidea). Zool. J. Linn. Soc. 154: 421-436.

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(20.) Lankester, E. R. 1875. Contributions to the developmental history of the Mollusca. Philos. Trans. R. Soc. Lond. 165: 1-48.

(21.) Krohn, A. 1853. On a new ciliated sail-bearing gastropod. (Translated from German) Archiv. Naturgesch.. Jahrg. 19, Bd. I, pp. 223-226.

(22.) Gegenbauer, C. 1855. Untersuchngen uber Pteropoden and Het-eropoden. Ein Beitrag zur Anatomie und Entwicklungsgeschichte dieser Tiere. Engelmann, Leipzig. [Investigations on Pteropods and Heteropods. A Contribution to the Anatomy and Ontogeny of These Animals. (Translated from German).]

(23.) Rouse, G. W. 1999. Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa. Biol. J. Linn. Soc. 66: 411-464.

(24.) Rouse, G. W. 2000. Polychaetes have evolved feeding larvae numerous times. Bull. Mar. Sci. 67: 391-409.

Received 12 March 2010; accepted 14 July 2010.

* To whom correspondence should be addressed. E-mail: kreynolds@mlml.calstate.edu

[dagger] First and second authors had equal contributions to these results. Discovery of the larval form was made independently by the American and Japanese teams.

KYLE C. REYNOLDS (1),*, [dagger], HIROMI WATANABE (2), [dagger], ELLEN E. STRONG (3), TAKENORI SASAKI (4), KATSUYUKI UEMATSU (5), HIROSHI MIYAKE (6), SHIGEAKI KOJIMA (7), YOHEY SUZUKI (8), KATSUNORI FUJIKURA (2), STACY KIM (1), AND CRAIG M. YOUNG (9)

(1) Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, California 95039; (2) Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima, Yokosuka 237-0061, Japan; (3) Smithsonian Institution, National Museum of Natural History, P.O. Box 37012, MRC 163, Washington, DC 20013-7012; (4) The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo 113-0033, Japan; (5) Marine Works Japan LTD, 2-15 Natsushima, Yokosuka 237-0061, Japan; (6) School of Marine Biosciences, Kitasato University, 160-4 Utou, Okkirai, Sanriku, Ofunato, Iwate 022-0101, Japan; Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan; (8) Advanced Industrial Science and Technology, 1-1-1 Umezono, Tsukuba, Ibaraki 305-8568, Japan; and (9) Oregon Institute of Marine Biology, University of Oregon, P.O. Box 5389, Charleston, Oregon 97420
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Author:Reynolds, Kyle C.; Watanabe, Hiromi; Strong, Ellen E.; Sasaki, Takenori; Uematsu, Katsuyuki; Miyake,
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:1USA
Date:Aug 1, 2010
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