Cryptic niche switching in a chemosymbiotic gastropod

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 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.

部分动物（包括两栖类与昆虫）的生活史差异极大，历史上曾被误认为是不同物种。"变态（Metamorphosis）"广义上涵盖生物体的显著形态变化，更重要的是伴随而来的营养策略转变。许多海洋动物具有双相生活史：小型浮游幼体需经历一次或多次变态转变，之后在底栖生境中定居并形成稳定的成体形态。定居后，热液喷口腹足类Gigantopelta chessoia会在体长约5-7毫米时经历一次隐秘的额外变态过程。其终末成体阶段完全依赖化能自养共生体；而体型较小的个体并不携带共生体，推测依靠刮食获取营养。本研究通过高分辨X射线显微断层扫描技术对生长序列样本的内部器官进行三维重建，结果显示：即便在体型微小但已性成熟的个体中，这种转变仍会极大地重构其内部器官，但外部形态无任何明显变化。我们提出"隐秘变态（cryptometamorphosis）"这一术语，用以描述这种与性成熟无关、仅发生内部解剖结构重塑的重大形态变化与营养策略转变的全新现象。生态系统的能量流动研究依赖于物种的摄食生态学；本研究凸显了成年动物可发生深刻的生物学转变并进而影响能量动态的可能性。