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Larval apical sensory organ in a neritimorph gastropod, an ancient gastropod lineage with feeding larvae

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Abstract

The Neritimorpha is an ancient clade of gastropods that may have acquired larval planktotrophy independently of the evolution of this developmental mode in other gastropods (caenogastropods and heterobranchs). Neritimorphs are therefore centrally important to questions about larval evolution within the Gastropoda, but there is very little information about developmental morphology through metamorphosis for this group. We used immunolabeling (antibodies binding to acetylated α-tubulin and serotonin) and serial ultrathin sections for transmission electron microscopy to characterize the apical sensory organ in planktotrophic larvae of a marine neritimorph. The apical sensory organ of gastropod larvae is a highly conserved multicellular sensory structure that includes an apical ganglion and often an associated ciliary structure. Surprisingly, the apical ganglion of Nerita melanotragus (Smith, 1884) does not have typical ampullary neurons, a type of sensory neuron consisting of a cilia filled inpocketing that has been described in all other major gastropod groups. N. melanotragus has cilia-filled pockets embedded within the apical ganglion, but these so-called “sensory cups” are cassettes of multiple cells: one supporting cell and up to three multiciliated sensory cells. We suggest that an internalized pocket that is filled with cilia and open to the exterior via a narrow pore may be essential architectural features for whatever sensory cues are detected by ampullary neurons and sensory cups; however, morphogenesis of these features at the cellular level has undergone evolutionary change. We also note a correlation between the number of sensory elements consisting of cilia-filled pockets within the larval apical sensory organ of gastropods and morphological complexity of the velum or length of the trochal ciliary bands.

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Acknowledgments

We thank Dr. Maria Byrne, University of Sydney, Australia for generously allowing use of her lab facilities within the Discipline of Anatomy and Histology, where larval neritimorphs were cultured. Mr. Brent Gowen did an expert job of cutting serial ultrathin sections used in this study. Funding for this research was provided by a Discovery Grant to LRP from NSERC of Canada.

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Correspondence to Louise R. Page.

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Page, L.R., Kempf, S.C. Larval apical sensory organ in a neritimorph gastropod, an ancient gastropod lineage with feeding larvae. Zoomorphology 128, 327–338 (2009). https://doi.org/10.1007/s00435-009-0093-9

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  • DOI: https://doi.org/10.1007/s00435-009-0093-9

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