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Phylogenetic constraint and phenotypic plasticity in the shell microstructure of vent and seep pectinodontid limpets

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Abstract

Pectinodontid limpets of the genus Bathyacmaea are endemic to hot vents and cold seeps and exhibit greatly variable shell and radular macro-morphologies, rendering reliable species-level identification challenging. Here, we analyzed shell microstructures of western Pacific vent/seep Bathyacmaea limpets using scanning electron microscopy and Raman spectrophotometry to test its usefulness in providing phylogenetic signals. Bathyacmaea shells comprised of two forms of calcitic microstructure including irregular spherulitic prismatic type-A (ISP type-A) and semi-foliated (SF), as well as the aragonitic crossed lamellar (CL) microstructure. Despite marked differences in macroscopic shell morphologies once leading them to be classified into different species or even genera, six morphotypes of Bathyacmaea nipponica from different chemosynthetic localities and substrates shared an outermost ISP-A layer and alternating layers of SF and CL structures in their outer and inner shell layers. A genetically divergent lineage recovered from the South Chamorro Seamount, however, differed in having a simple three-layered shell composition consisting of ISP-A, SF, and CL structures, in that order, from the outside, and an unusually thin inner shell layer consisting of only CL structure. Moreover, the ratio of aragonite and calcite varied with habitat conditions, with calcite dominating in vents and aragonite dominating in seeps. These results suggest that the shell microstructure of pectinodontids is under phylogenetic constraints and provides useful taxonomic signals, while the mineral polymorphism in aragonite/calcite ratio varies according to environmental factors. Furthermore, microstructures of two ‘species’ from Cretaceous seeps confirmed the same patterns in fossil lineages.

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Data availability

The datasets generated during and/or analysed during the current study are available in the NCBI GenBank repository, with accession numbers MN631154-MN631157, MN634249-MN634250, MN658524, MN688133, MN715828-MN715829, MT275737-MT275738, and MT309592-309593. Specimens used in the present study are deposited in the Department of Historical Geology and Paleontology in the University Museum, the University of Tokyo.

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Acknowledgements

We thank captains and crews of R/Vs NATSUSHIMA, SHINSEI-MARU, JOIDES RESOLUTION, and XIANGYANGHONG 9, as well as pilots of ROVs Hyper-Dolphin and KAIKO, and DSV Jiaolong for their sampling efforts. Cruise principal scientists are gratefully acknowledged: Ken Takai, NT15-13; Akinori Yabuki, KS-16-04; Patricia Fryer, IODP/JOIDES RESOLUTION Expedition 366; Feng Liu/Huaiyang Zhou, Dayang-31. Ryoko Yamazaki (JAMSTEC) assisted in sequencing of pectinodontid limpets. Ting Xu and Jianwen Qiu (Hong Kong Baptist University) and thanked for providing specimens from the South China Sea used in this study. Ken Takai (JAMSTEC) kindly collected pectinodontid limpets from a steel pipe recovered from the South Chamorro Seamount during IODP expedition 366 and provided the specimens to us. Our Raman analysis was technically supported by Tatsuhiko Kawamoto (Shizuoka University). Masaki Takaya (Kyoto University) helped our petrographic investigation. We thank the editor, Dr. Elizabeth M. Harper, and an anonymous reviewer for their constructive criticism and useful suggestions. HKW and CC were supported by a JSPS Grant-in-Aid (18K06401), and RGJ was supported by JSPS Grant-in-Aid (26287131, 15H04412, and 16H05740).

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  1. Waseda University, 1-6-1, Nishi-Waseda, Shinjyuku-ku, Tokyo, 169-8050, Japan

    Kei Sato

  2. The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 110-0033, Japan

    Kei Sato

  3. X-STAR, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan

    Hiromi Kayama Watanabe & Chong Chen

  4. Kanazawa University, Kakuma, Kanazawa, Ishikawa, 920-1192, Japan

    Robert G. Jenkins

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  1. Kei Sato
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Correspondence to Kei Sato.

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Sato, K., Watanabe, H.K., Jenkins, R.G. et al. Phylogenetic constraint and phenotypic plasticity in the shell microstructure of vent and seep pectinodontid limpets. Mar Biol 167, 79 (2020). https://doi.org/10.1007/s00227-020-03692-z

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