Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T11:11:28.280Z Has data issue: false hasContentIssue false
  • English
  • Français

Shell variations in the gastropod, Monodonta labio, in the North-western Pacific: the important role of temperature in the evolution process

Published online by Cambridge University Press:  24 June 2019

Dan Zhao ,
Ling-Feng Kong ,
Takenori Sasaki  and
Qi Li
Dan Zhao
Affiliation:
Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China The University Museum, The University of Tokyo, Tokyo 113-0033, Japan
Ling-Feng Kong
Affiliation:
Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China
Takenori Sasaki
Affiliation:
The University Museum, The University of Tokyo, Tokyo 113-0033, Japan
Qi Li*
Affiliation:
Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China
*
Author for correspondence: Qi Li, E-mail: qili66@ouc.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Molluscan shells showing phenotypic variations are ideal models for studying evolution and plasticity. In north-eastern Asia, genetic and morphological diversity of the gastropod, Monodonta labio, were assumed to be influenced by both palaeoclimatic changes and current ecological factors. In this study, we examined spatial variations in shell shape of M. labio using general measurement and geometric morphometric analysis. We also investigated whether shell shape variation is best explained by environmental gradients or by genetic structuring, based on our prior molecular phylogeographic study. Two common morphological forms were observed among Chinese populations and in the adjacent Asian areas. Both the analyses revealed separation patterns in morphological variations of shell shape among the clades and populations. Environmental modelling analysis showed a significant correlation between shape variations and local maximum temperatures of the warmest month, indicating the role of natural selection in the evolution of this species. Data obtained in this study, combined with the cytochrome oxidase subunit I (COI) molecular phylogenetic data from the prior study, showed that morphological variations in M. labio were constrained by both local adaptation and phenotypic plasticity. We hypothesized that geographic separation by the Dongshan Landbridge was the first step towards its diversification, and that the temperature gradient between the East China Sea and South China Sea probably was the selective force driving the divergence of its morphological variations.

Keywords

AdaptationGastropodanatural selectionphenotypic plasticitytemperatureNorth-western Pacific
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 7 , November 2019 , pp. 1591 - 1599
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, DC and Collyer, ML (2009) A general framework for the analysis of phenotypic trajectory studies. Evolution 63, 1143–1154.Google Scholar
Agrawal, AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294, 321–326.Google Scholar
Avaca, MS, Narvarte, M, Martín, P and Molen, S (2013) Shell shape variation in the Nassariid Buccinanops globulosus in northern Patagonia. Helgoland Marine Research 67, 567–577.Google Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2014) Lme4: linear mixed-effects models using Eigen and S4. R package version 1, 1–23.Google Scholar
Briggs, JC (1995) Global Biogeography. Amsterdam: Elsevier Science B.V.Google Scholar
Carvajal-Rodríguez, A, Conde-Padín, P and Rolán-Alvarez, E (2005) Decomposing shell form into size and shape by geometric morphometric methods in two sympatric ecotypes of Littorina saxatilis. Journal of Molluscan Studies 71, 313–318.Google Scholar
Climate Data Guide. World Ocean Atlas 2013. Available at https://climatedataguide.ucar.edu/climate-data/world-ocean-atlas-2013-woa13.Google Scholar
Chin, IM (2003) Variation in Monodonta labio among different intertidal habitats in Hong Kong (PhD thesis). The University of Hong Kong, Hong Kong.Google Scholar
Coan, EV, Lutaenko, KA, Zhang, J and Sun, Q (2015) The molluscan taxa of A. W. Grabau & S. G. King (1928). Malacologia 58, 179–224.Google Scholar
Daniel, F, Cleary, R, Descimon, H and Menken, SB (2002) Genetic and ecological differentiation between the butterfly sister species Colias alfacariensis and Colias hyale. Contributions to Zoology 71, 131–139.Google Scholar
Dowle, EJ, Morgan-Richards, M, Brescia, F and Trewick, SA (2015) Correlation between shell phenotype and local environment suggests a role for natural selection in the evolution of Placostylus snails. Molecular Ecology 24, 4205–4221.Google Scholar
Forrester, GE, MacFarlan, RJ, Holevoet, AJ and Merolla, S (2016) Dislodgement force and shell morphology vary according to wave exposure in a tropical gastropod (Cittarium pica). Marine Biology Research 12, 986–992.Google Scholar
Grabau, AW and King, SG (1928) Shells of Peitaiho. Beijing: Peking and The Peking Leader Press.Google Scholar
Higo, SI, Callomon, P and Goto, Y (1999) Catalogue and Bibliography of the Marine Shell-Bearing Mollusca of Japan. Osaka: Elle Scientific.Google Scholar
Hijmans, RJ, Guarino, L, Cruz, M and Rojas, E (2001) Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127, 15–19.Google Scholar
Hijmans, RJ, Cameron, SE, Parra, JL, Jones, PG and Jarvis, A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.Google Scholar
Hollander, J and Butlin, RK (2010) The adaptive value of phenotypic plasticity in two ecotypes of a marine gastropod. BMC Evolutionary Biology 10, 333.Google Scholar
Irie, T (2005) Geographical variation of shell morphology in Cypraea annulus (Gastropoda: Cypraeidae). Journal of Molluscan Studies 72, 31–38.Google Scholar
Johannesson, K, Johannesson, B and Rolan-Alvarez, E (1993) Morphological differentiation and genetic cohesiveness over a microenvironmental gradient in the marine snail Littorina saxatilis. Evolution 47, 1770–1787.Google Scholar
Johnson, MS and Black, R (2008) Adaptive responses of independent traits to the same environmental gradient in the intertidal snail Bembicium vittatum. Heredity 101, 83–91.Google Scholar
Klingenberg, CP (2011) Morphoj: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–357.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.Google Scholar
Morphometrics at SUNY Stony Brook. Computer program, Department of Ecology & Evolution and Anthropology, State University of New York, Stony Brook. Available at life.bio.sunysb. edu/morph/.Google Scholar
Ni, G, Li, Q, Kong, L and Yu, H (2014) Comparative phylogeography in marginal seas of the northwestern Pacific. Molecular Ecology 23, 534–548.Google Scholar
Ocean data view. Computer program. Available at http://odv.awi.de.Google Scholar
Preston, SJ and Roberts, D (2007) Variation in shell morphology of Calliostoma zizyphinum (Gastropoda: Trochidae). Journal of Molluscan Studies 73, 101–104.Google Scholar
Rundle, HD and Nosil, P (2005) Ecological speciation. Ecology Letters 8, 336–352.Google Scholar
Schluter, D and Conte, GL (2009) Genetics and ecological speciation. Proceedings of the National Academy of Sciences USA 106, 9955–9962.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671.Google Scholar
Shen, KN, Jamandre, BW, Hsu, CC, Tzeng, WN and Durand, JD (2011) Plio-Pleistocene sea level and temperature fluctuations in the northwestern Pacific promoted speciation in the globally-distributed flathead mullet Mugil cephalus. BMC Evolutionary Biology 11, 83.Google Scholar
Solas, M, Sepúlveda, R and Brante, A (2013) Genetic variation of the shell morphology in Acanthina monodon (Gastropoda) in habitats with different wave exposure conditions. Aquatic Biology 18, 253–260.Google Scholar
Takenouchi, K (1985) An analysis of shell character and distribution of the intertidal trochid, Monodonta labio (Linné) (Gastropoda: Prosobranchia). Japanese Journal of Malacology 44, 110–122. In Japanese with English abstract.Google Scholar
Tamaki, K and Honza, E (1991) Global tectonics and formation of marginal basins – role of the western Pacific. Episodes 14, 224–230.Google Scholar
Team RC (2017) R: A Language and Environment for Statistical Computing. Available at http://www.r-project.org. Vienna: R Foundation.Google Scholar
Trussell, GC (2000) Phenotypic clines, plasticity, and morphological trade-offs in an intertidal snail. Evolution 54, 151–166.Google Scholar
Trussell, GC, Johnson, AS, Rudolph, SG and Gilfillan, ES (1993) Resistance to dislodgement: habitat and size-specific differences in morphology and tenacity in an intertidal snail. Marine Ecology Progress Series 100, 135–144.Google Scholar
Vavrek, MJ (2011) Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontologia Electronica 14, 16.Google Scholar
Vermeij, GJ (1973) Morphological patterns in high-intertidal gastropods: adaptive strategies and their limitations. Marine Biology 20, 319–346.Google Scholar
Vermeij, GJ (1987) Evolution and Escalation: An Ecological History of Life. Princeton, NJ: Princeton University Press.Google Scholar
Wang, L (1994) Sea surface temperature history of the low latitude western Pacific during the last 5.3 million years. Palaeogeography, Palaeoclimatology, Palaeoecology 108, 379–436.Google Scholar
Wang, X, Xu, H, Zou, L, Du, X, Wang, FL, Zheng, W, Han, ZQ and Shui, BN (2013) Morphological variation analysis of three different geographic populations of Monodonta labio. South China Fisheries Science 9, 22–27. In Chinese with English abstract.Google Scholar
Watson, SA, Peck, LS, Tyler, PA, Southgate, PC, Tan, KS, Day, RW and Morley, SA (2012) Marine invertebrate skeleton size varies with latitude, temperature and carbonate saturation: implications for global change and ocean acidification. Global Change Biology 18, 3026–3038.Google Scholar
Wong, YM and Lim, SSL (2017) Influence of shell morphometry, microstructure, and thermal conductivity on thermoregulation in two tropical intertidal snails. Invertebrate Biology 136, 228–238.Google Scholar
WorldClim–Global Climate Data. WorldClim 1.4: Current conditions (~1960–1990). Bioclimatic variables. Available at http://www.worldclim.org.Google Scholar
Yamazaki, D, Miura, O, Ikeda, M, Kijima, A, Sasaki, T and Chiba, S (2017) Genetic diversification of intertidal gastropoda in an archipelago: the effects of islands, oceanic currents, and ecology. Marine Biology 164, 184.Google Scholar
Yeaman, S, Hodgins, KA, Lotterhos, KE, Suren, H, Nadeau, S, Degner, JC, Nurkowski, KA, Smets, P, Wang, T, Gray, LK, Liepe, KJ, Hamann, A, Holliday, JA, Whitlock, MC, Rieseberg, LH and Aitken, SN (2016) Convergent local adaptation to climate in distantly related conifers. Science 353, 1431–1433.Google Scholar
Zelditch, M, Swiderski, D, Sheets, H and Fink, W (2004) Geometric Morphometrics for Biologists: A Primer. London: Elsevier.Google Scholar
Zhao, D, Li, Q, Kong, L and Yu, H (2017) Cryptic diversity of marine gastropod Monodonta labio (Trochidae): did the early Pleistocene glacial isolation and sea surface temperature gradient jointly drive diversification of sister species and/or subspecies in the Northwestern Pacific? Marine Ecology 38, e12443.Google Scholar
Supplementary material: File

Zhao et al. supplementary material

Zhao et al. supplementary material 1

Download Zhao et al. supplementary material(File)
File 62.9 KB