By more ways than one: Rapid convergence at hydrothermal vents shown by 3D anatomical reconstruction of Gigantopelta (Mollusca: Neomphalina)

BMC Evolutionary Biology

Research Article

Katrin Linse¹  Julia D. Sigwart²  Chong Chen³  Katsuyuki Uematsu⁴ 

[1] British Antarctic Survey, High Cross, Cambridge, UK;Marine Laboratory, Queen’s University Belfast, 12-13 The Strand, Portaferry, Northern Ireland;Berkeley, Museum of Paleontology, University of California, VLSB 1101, 94720, Berkeley, CA, USA;Marine Laboratory, Queen’s University Belfast, 12-13 The Strand, Portaferry, Northern Ireland;Department of Subsurface Geobiological Analysis and Research (D-SUGAR), Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima, 237-0061, Yokosuka, Kanagawa, Japan;Marine Works Japan Ltd., 3-54-1 Oppamahigashi, 237-0063, Yokosuka, Japan;

关键词: Adaptation;    Anatomy;    Convergence;    Evolution;    Extreme environment;    Symbiosis;   

DOI  :  10.1186/s12862-017-0917-z

 received in 2016-11-15, accepted in 2017-02-17,  发布年份 2017

来源: Springer

【 摘 要 】

BackgroundExtreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the ‘scaly-foot gastropod’ Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs.ResultsTransmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic.ConclusionsKey anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont’s adaptations to an extreme environment, are driven by optimising bacteria’s access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.

【 授权许可】

CC BY   
© The Author(s). 2017