Specification of polymorphism and classification of shell coloration in gastropods by the example of Littorina obtusata (Gastropoda: Littorinidae)
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Abstract
Understanding the patterns of microevolutionary processes involves a wide range of population genetic studies on different species. However, the number of genetically studied species is limited due to significant methodological difficulties in testing the genetic conditionality of various traits. Developing population phenetics may become an alternative, which allows considering a large number of new species subject to development of morphologically and genetically-based system to describe the variability and classification of phenotypic traits. Gastropods are a classic object for carrying out population genetic studies based on the analysis of polymorphism of shell coloration. The parametric classification system proposed by S. Sergievsky et al. (1995) for periwinkles of the genus Littorina may serve as a basis for the developing of a universal system for classifying color traits for that taxonomic group. Since a large amount of new data has been published in recent years, this system requires correction and revision. The study aims to revise the system, taking into account new material on the pigment composition, as well as on the peculiarities of the formation and inheritance of color traits, their joint occurrence, etc. A revised and modified classification system for shell coloration traits is presented by the example of the White Sea gastropods L. obtusata; this system considers the idea of the formation of a phenotype as a combination of several elementary traits. These are traits associated with the formation of: 1) a shell background color (the ability to include different pigments in the ostracum and the hypostracum color); 2) a pattern of spots (the presence of inclusions of white and/or brown pigment); and 3) wide longitudinal bands (brown, white, and orange). Elementary traits are highlighted taking into account the pigments involved, as well as the mechanisms of their formation and inheritance. When describing the shell coloration, elementary traits are first used to describe relatively simple traits (groups of phenes “Shell background color”, “Hypostracum color”, “Pattern of spots”, and “Wide longitudinal bands”), which are subsequently combined to describe the phenotype as a whole. Our study provides an overview of the available data on the qualitative composition of shell pigments in periwinkles and patterns of formation and inheritance of color traits; their possible combinations are described. The phenes isolated by us are described together with their occurrence, color specification in the RGB system, and the peculiarities of the formation, taking into account the distribution of pigments in the shell. Visible traits, that may be used to assess the distribution of pigments in the shell, are indicated. The ontogenetic changes in traits are described. Despite the fact that the proposed classification system is developed by the example of L. obtusata, it can be used for same purposes for other periwinkle species and, with some modifications, for a wide range of gastropod species.
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References
Бриттон Г. Биохимия природных пигментов. Москва : Мир, 1986. 422 с. [Britton G. The Biochemistry of Natural Pigments. Moscow : Mir, 1986, 422 p. (in Russ.)]
Козминский Е. В. Состояние популяций и зараженность Littorina saxatilis (Olivi, 1792) и L. obtusata (Linnaeus, 1758) в Южной губе о. Ряжков в 2005 г. / Летопись природы Кандалакшского заповедника за 2005 год. Т. 2 / ред. А. С. Корякин. Кандалакша, 2006. С. 100–114. [Kozminskii E. V. Conditions of Littorina saxatilis (Olivi, 1792) and L. obtusata (Linnaeus, 1758) populations and structure of parasite invasions in these species in Yuznaya inlet of Ryashkov Island in 2006. In: The Chronicle of Nature by the Kandalaksha Reserve for 2005. Vol. 2 / A. S. Koryakin (Ed.). Kandalaksha, 2006, pp. 100–114. (in Russ.)]
Козминский Е. В. Изучение наследования продольных полос на раковине у моллюсков Littorina obtusata и Littorina saxatilis (Gastropoda, Prosobranchia) // Генетика. 2011. Т. 47, № 8. С. 1112–1119. [Kozminsky E. V. Inheritance of longitudinal shell bands in the snails Littorina obtusata and Littorina saxatilis (Gastropoda, Prosobranchia). Russian Journal of Genetics, 2011, vol. 47, no. 8, pp. 987–993. (in Russ.)]. https://doi.org/10.1134/S1022795416080068
Козминский Е. В. Особенности наследования фоновой окраски раковины у моллюсков Littorina obtusata (Gastropoda, Littorinidae) // Генетика. 2014. Т. 50, № 10. С. 1177–1187. [Kozminsky E. V. Inheritance of the background shell color in the snails Littorina obtusata (Gastropoda, Littorinidae). Russian Journal of Genetics, 2014, vol. 50, no. 10, pp. 1038–1047. (in Russ.)]. https://doi.org10.7868/S0016675814100051
Козминский Е. В. Наследование продольных белых полос на раковине у моллюсков Littorina obtusata (Gastropoda, Prosobranchia) // Генетика. 2016. Т. 52, № 8. С. 991–995. [Kozminsky E. V. Inheritance of longitudinal white stripes on the shell of mollusks Littorina obtusata (Gastropoda, Prosobranchia). Russian Journal of Genetics, 2016, vol. 52, no. 8, pp. 882–886. (in Russ.)]. https://doi.org/10.7868/S0016675816080063
Козминский Е. В. Состояние популяций и зараженность Littorina saxatilis (Olivi, 1792) и L. obtusata (Linnaeus, 1758) в Южной губе о. Ряжков в 2017 и 2018 гг. // Летопись природы Кандалакшского заповедника за 2019 год. Т. 2 / ред. Е. Л. Толмачева. Кандалакша, 2020. С. 62–79. [Kozminsky E. V. Conditions of Littorina saxatilis (Olivi, 1792) and L. obtusata (Linnaeus, 1758) populations and structure of parasite invasions in these species in Yuznaya inlet of Ryashkov Island in 2017 and 2018. In: The Chronicle of Nature by the Kandalaksha Reserve for 2019. Vol. 2 / E. L. Tolmacheva (Ed.). Kandalaksha, 2020, pp. 62–79. (in Russ.)]
Козминский Е. В., Лезин П. А. Методика цветовых измерений элементов окраски раковины у брюхоногих моллюсков // Биология моря. 2006. Т. 32, № 5. С. 371–373. [Kozminskii E. V., Lezin P. A. Method of color measurements of the elements of color in gastropod shell. Russian Journal of Marine Biology, 2006, vol. 32, no. 5, pp. 316–318. (in Russ.)]. https://doi.org/10.1134/S1063074006050105
Козминский Е. В., Лезин П. А. Распределение пигментов в раковине брюхоногого моллюска Littorina obtusata (Linnaeus, 1758) // Биология моря. 2007. Т. 33, № 4. С. 284–290. [Kozminsky E. V., Lezin P. A. Distribution of pigments in the shell of the gastropod Littorina obtusata (Linnaeus, 1758). Russian Journal of Marine Biology, 2007, vol. 33, no. 4, pp. 238–244. (in Russ.)]. https://doi.org/10.1134/S1063074007040062
Козминский Е. В., Гранович А. И., Сергиевский С. О. Наследование признаков окраски раковины у Littorina saxatilis (Olivi) (Gastropoda: Prosobranchia) // Труды Зоологического института. 1995. Т. 264. С. 19–34. [Kozminsky E. V., Granovitch A. I., Sergievsky S. O. Inheritance of shell colour morphs of Littorina saxatilis (Olivi) (Gastropoda: Prosobranchia). Trudy Zoologicheskogo instituta, 1995, vol. 264, pp. 19–34. (in Russ.)]
Козминский Е. В., Лезин П. А., Фокин М. В. Методика изучения наследования признаков окраски раковины у моллюсков рода Littorina (Gastropoda, Prosobranchia) // Зоологический журнал. 2008. Т. 87, № 5. С. 614–619. [Kozminsky E. V., Lezin P. A., Fokin M. V. A methodology of studying the inheritance of shell color in mollusks of the genus Littorina (Gastropoda, Prosobranchia). Zoologicheskii zhurnal, 2008, vol. 87, no. 5, pp. 614–619. (in Russ.)]
Козминский Е. В., Лезин П. А., Фокин М. В. Изучение наследования рисунка из белых пятен на раковине у Littorina obtusata (Gastropoda, Prosobranchia) // Генетика. 2010. Т. 46, № 12. С. 1652–1659. [Kozminskii E. V., Lezin P. A., Fokin M. V. A study of inheritance of white spots on the shell of Littorina obtusata (Gastropoda, Prosobranchia). Russian Journal of Genetics, 2010, vol. 46, no. 12, pp. 1455–1461. (in Russ.)]. https://doi.org/10.1134/S1022795410120082
Лезин П. А., Козминский Е. В. Цветовые характеристики элементов окраски раковины Littorina obtusata (Gastropoda: Prosobranchia) и эффективность их использования при выделении фенотипических групп // Зоологический журнал. 2008. Т. 87, № 1. С. 29–35. [Lezin P. A., Kozminskii E. V. Color characteristics of Littorina obtusata (Gastropoda, Prosobranchia) shells and their use for distinguishing its phenotypic groups. Zoologicheskii zhurnal, 2008, vol. 87, no. 1, pp. 29–35. (in Russ.)]
Сергиевский С. О., Гранович А. И., Козминский Е. В. Полиморфизм окраски раковины Littorina saxatilis (Olivi): принципы классификации // Труды Зоологического института. 1995. Т. 264. С. 3–18. [Sergievsky S. O., Granovitch A. I., Kozminsky E. V. Shell colour polymorphism of Littorina saxatilis (Olivi): Classification principles. Trudy Zoologicheskogo instituta, 1995, vol. 264, pp. 3–18. (in Russ.)]
Яблоков А. В. Популяционная биология. Москва : Высшая школа, 1987. 303 с. [Yablokov A. V. Populyatsionnaya biologiya. Moscow : Vysshaya shkola, 1987, 303 p. (in Russ.)]
Яблоков А. В., Ларина Н. И. Введение в фенетику популяций. Москва : Высшая школа, 1985. 159 с. [Yablokov A. V., Larina N. I. Vvedenie v fenetiku populyatsii. Moscow : Vysshaya shkola, 1985, 159 p. (in Russ.)]
Backeljau T., Baur A., Baur B. Population and conservation genetics. In: The Biology of Terrestrial Molluscs / G. M. Barker (Ed.). Wallingford, UK : CAB International Publishing, 2001, pp. 383–412.
Bevelander G., Nakahara H. An electron microscope study of the formation and structure of the periostracum of a gastropod, Littorina littorea. Calcified Tissue Research, 1970, vol. 5, no. 1, pp. 1–12. https://doi.org/10.1007/BF02017528
Comfort A. Biochemistry of molluscan shell pigments. Journal of Molluscan Studies, 1950, vol. 28, iss. 2-3, pp. 79–85. https://doi.org/10.1093/oxfordjournals.mollus.a064570
Comfort A. Observations on the shell pigments of land pulmonates. Journal of Molluscan Studies, 1951, vol. 29, pp. 35–44. https://doi.org/10.1093/oxfordjournals.mollus.a064598
Cook L. M. The genetics of Cepaea nemoralis. Heredity, 1967, vol. 22, no. 3, pp. 397–410. https://doi.org/10.1038/hdy.1967.49
Cook L. M., King J. M. B. Some data on the genetics of shell-character polymorphism in the snail Arianta arbustorum. Genetics, 1966, vol. 53, iss. 3, pp. 415–425. https://doi.org/10.1093/genetics/53.3.415
Délé-Dubois M.-L., Merlin J.-C. Étude par spectroscopie Raman de la pigmentation du squelette calcaire du corail. Revue de Gemmologie, 1981, vol. 68, pp. 10–13.
Estévez D., Kozminsky E., Carvajal-Rodríguez A., Caballero A., Faria R., Galindo J., Rolán-Alvarez E. Mate choice contributes to the maintenance of shell color polymorphism in a marine snail via frequency-dependent sexual selection. Frontiers in Marine Science, 2020, vol. 7, art. no. 614237 (15 p.). https://doi.org/10.3389/fmars.2020.614237
Hedegaard G., Bardeau J.-F., Ghateigner D. Molluscan shell pigments: An in situ resonance raman study. Journal of Molluscan Studies, 2006, vol. 72, no. 2, pp. 157–162. https://doi.org/10.1093/mollus/eyi062
Ito S., Konuma J. Disruptive selection of shell colour in land snails: A mark–recapture study of Euhadra peliomphala simodae. Biological Journal of the Linnean Society, 2020, vol. 129, no. 2, pp. 323–333. https://doi.org/10.1093/biolinnean/blz168
Lucas M. Pigments in Mollusca. Conchiglia, 1974, vol. 6, pp. 5–10.
Miura O., Nishi S., Chiba S. Temperature-related diversity of shell colour in the intertidal gastropod Batillaria. Journal of Molluscan Studies, 2007, vol. 73, no. 3, pp. 235–240. https://doi.org/10.1093/mollus/eym019
Murray J. The genetics of the Mollusca. In: Handbook of Genetics. Vol. 3. Invertebrates of Genetic Interest / R. C. King (Ed.). New York : Plenum Press, 1975, pp. 3–31.
Pettitt C. W. A proposed new method of scoring the colour morphs of Littorina saxatilis (Olivi, 1772) (Gastropoda: Prosobranchia). Journal of Molluscan Studies, 1973, vol. 40, no. 6, pp. 531–538. https://doi.org/10.1093/oxfordjournals.mollus.a065247
Reid D. G. Systematics and Evolution of Littorina. Dorchester, England, UK : Dorset Press, 1996, 463 p.
Reimchen T. E. Substratum heterogeneity, crypsis, and colour polymorphism in an intertidal snail (Littorina mariae). Canadian Journal of Zoology, 1979, vol. 57, no. 5, pp. 1070–1085. https://doi.org/10.1139/z79-135
Rolán-Alvarez E., Austin C. J., Boulding E. G. The contribution of the genus Littorina to the field of evolutionary ecology. In: Oceanography and Marine Biology: An Annual Review / D. J. Hughes, A. C. Dale, R. N. Hughes, I. P. Smith (Eds). Boca Raton : CRC Press, 2015, vol. 53, pp. 157–214. https://doi.org/10.1201/b18733
Sacchi C. F. Le polychromatisme des littorines (Gasteropodes, Prosobranches) d’Europe: points de vue d’un ecologiste. Mémoires de la Société zoologique de France, 1974, vol. 37, pp. 75–84.
Scheil A. E., Hilsmann S., Triebskorn R., Köhler H.-R. Shell colouration and parasite tolerance in two helicoid snail species. Journal of Invertebrate Pathology, 2014, vol. 117, pp. 1–8. https://doi.org/10.1016/j.jip.2014.01.003
Sokolova I. M., Berger V. Ja. Physiological variation related to shell colour polymorphism in White Sea Littorina saxatilis. Journal of Experimental Marine Biology and Ecology, 2000, vol. 245, iss. 1, pp. 1–23. https://doi.org/10.1016/S0022-0981(99)00132-X
Williams S. T. Molluscan shell colour. Biological Reviews, 2017, vol. 92, iss. 2, pp. 1039–1058. https://doi.org/10.1111/brv.12268
Williams S. T., Ito S., Wakamatsu K., Goral T., Edwards N. P., Wogelius R. A., Henkel T., de Oliveira L. F. C., Maia L. F., Strekopytov S., Jeffries T., Speiser D. I., Marsden J. T. Identification of shell colour pigments in marine snails Clanculus pharaonius and C. margaritarius (Trochoidea; Gastropoda). PLoS ONE, 2016, vol. 11, no. 7, art. no. e0156664 (25 p.). https://doi.org/10.1371/journal.pone.0156664
