Cryptic niche switching in a chemosymbiotic gastropod

Author:

Chen Chong1ORCID,Linse Katrin2,Uematsu Katsuyuki3,Sigwart Julia D.45ORCID

Affiliation:

1. Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, Kanagawa 2370061, Japan

2. British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, UK

3. Marine Works Japan Ltd., 3-54-1 Oppamahigashi, Yokosuka, Kanagawa 2370063, Japan

4. Marine Laboratory, Queen's University Belfast, 12-13 The Strand, Portaferry BT22 1PF, N. Ireland

5. Museum of Paleontology, University of California, Berkeley, CA 94720, USA

Abstract

Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm . The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flow in ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics.

Funder

Japan Synchrotron Radiation Research Institute / SPring-8

Lawrence Berkeley National Laboratory

Natural Environment Research Council

H2020 Marie Skłodowska-Curie Actions

Japan Society for the Promotion of Science

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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