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How did phytoplankton-feeding larvae re-evolve within muricid gastropods? A view from developmental morphology

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Abstract

Post-Paleozoic life history transitions in mollusks and echinoderms have been biased toward switches from feeding, planktonic larvae (planktotrophic), to one of the non-feeding developmental modes, such as maternally provisioned planktonic larvae, fully encapsulated larvae, or direct development. Nevertheless, rare resurrections of feeding larvae from fully encapsulated larvae have occurred within calyptraeid and muricid gastropods. The only previous study on the developing foregut of a muricid with encapsulated larvae (Nucella lapillus) indicated loss of the larval esophagus, a potential barrier to evolutionary re-emergence of larval planktotrophy. However, histological and ultrastructural examination of foregut development in two other nucellids, Nucella lamellosa and N. ostrina, both with fully encapsulated development, revealed a transient larval esophagus in both, as identified by anatomical position, tissue composition, interconnections to other structures, and fate at metamorphosis. The larval esophagus is difficult to recognize in nucellids without a comparative framework and a complete developmental series extending from early veliger stages through to juveniles. Both the larval mouth and distal larval esophagus are completely destroyed at metamorphosis. Surprisingly, encapsulated larvae of N. lamellosa also developed all three velar ciliary tracts needed for capture and ingestion of particles, despite absence of nurse egg feeding by encapsulated larvae of this species and despite apparent absence of phytoplankton-feeding larvae in this genus since its origin 20 million years ago. Retention of a larval esophagus and a full complement of velar ciliary tracts needed for particle capture and ingestion in encapsulated larvae of some muricids may help explain how larval planktotrophy re-emerged within this clade.

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Acknowledgments

We thank Brent Gowen of the University of Victoria’s Electron Microscopy Laboratory for assistance with scanning electron microscopy. Funding was provided by the Natural Sciences and Engineering Research Council of Canada by way of a postgraduate scholarship to BH and a Discovery Grant (RGPIN138169-2009) to LRP.

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Funding was provided by the Natural Sciences and Engineering Research Council of Canada by way of a postgraduate scholarship awarded to BH and a Discovery Grant (RGPIN138169-2009) to LRP.

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  1. Department of Biology, University of Victoria, P.O. Box 1700, STN CSC, Victoria, BC, V8W 2Y2, Canada

    Brenda Hookham & Louise R. Page

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  1. Brenda Hookham
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Hookham, B., Page, L.R. How did phytoplankton-feeding larvae re-evolve within muricid gastropods? A view from developmental morphology. Mar Biol 163, 11 (2016). https://doi.org/10.1007/s00227-015-2784-8

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