Instability of the Mother’s Environment Leads to Reduced Developmental Robustness in  Lymnaea stagnalis  (Mollusca: Gastropoda)

A. I. Bogomolov; Богомолов А. И.; Y. A. Kraus; Краус Ю. А.; E. E. Voronezhskaya; Воронежская Е. Е.

doi:10.31857/S047514502305004X

Instability of the Mother’s Environment Leads to Reduced Developmental Robustness in Lymnaea stagnalis (Mollusca: Gastropoda)

作者: Bogomolov A.I.¹^,2, Kraus Y.A.¹^,2, Voronezhskaya E.E.²
隶属关系:
1. Faculty of Biology, Lomonosov Moscow State University
2. Koltzov Institute of Developmental Biology of the Russian Academy of Sciences
期: 卷 54, 编号 5 (2023)
页面: 358-367
栏目: Short communications
URL: https://journals.rcsi.science/0475-1450/article/view/137069
DOI: https://doi.org/10.31857/S047514502305004X
EDN: https://elibrary.ru/KICFMT
ID: 137069

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详细

Adaptive maternal effects that increase the adaptability of offspring are often caused by stressful conditions that persist in the environment for an extended period of time. The question arises, what is the threshold at which maternal effects cease to be adaptive for offspring and lead to developmental disorders? One of the stressors is considered to be unpredictable changes in environmental conditions. We aimed to test whether a mother’s inhabitation of unstable environment could lead to a decrease of developmental robustness in the embryos of the gastropod mollusk Lymnaea stagnalis. The laboratory population of snails was split into two groups. For the first group, conditions were maintained as stable as possible, with constant water exchange and excessive feeding. The second group was kept under unstable (stressful) conditions, with episodic feeding and water exchange. It turned out that unstable conditions alone did not affect the frequency of developmental anomalies in the offspring. Since serotonin is presumably plays the role of the signaling molecule mediating the maternal effect in L. stagnalis, we subjected embryos of both groups to the biochemical precursor of serotonin (5-HTP). After incubation in 5-HTP, the proportion of embryos with developmental anomalies was significantly higher among the offspring of mothers living in unstable conditions. We confirmed the important role of serotonin as a factor mediating communication between the organisms of mother and offspring by revealing serotoninergic innervation of the hermaphroditic gland (ovotestis) and accumulation of serotonin in the cytoplasm of forming oocytes. Our experiments suggest that under the stressful environmental conditions, serotonin accumulation by the oocyte/zygote may increase to a maladaptive level and lead to a decrease in the robustness of embryonic development.

关键词

maternal effects, developmental robustness, developmental anomalies, serotonin, Gastropoda, Lymnaea stagnalis

参考

Bogomolov A.I., Voronezhskaya E.E. An increase in the level of intracellular serotonin in blastomeres leads to the disruption in the spiral cleavage pattern in the mollusc Lymnaea stagnalis // Russian J. Dev. Bio. 2022. V. 53. №. 2. P. 115–120. https://doi.org/10.1134/S1062360422020035
Dantzer B., Boutin S., Lane J.E., McAdam A.G. Integrative studies of the effects of mothers on offspring: an example from wild North American red squirrels // Advances in Neurobiology / Ed. González-Mariscal G. 2022. V. 27. P. 269–296. Springer: Cham. https://doi.org/10.1007/978-3-030-97762-7_9
Dantzer B., Newman A.E., Boonstra R., Palme R., Boutin S., Humphries M.M., McAdam A.G. Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal // Science. 2013. V. 340(6137). P. 1215–1217.
Ivashkin E., Khabarova M.Y., Melnikova V., Nezlin L.P., Kharchenko O., Voronezhskaya E.E. et al. Serotonin mediates maternal eﬀects and directs developmental and behavioral changes in the progeny of snails // Cell Rep. 2015. V. 12. P. 1144–1158. https://doi.org/10.1016/j.celrep.2015.07.022
Joosse J., Boer H.H., Comelisse C.J. Gametogenesis and oviposition in Lymnaea stagnalis as influenced by Y-irradiation and hunger // Symp. Zoo 1. Soc. London. 1968. V. 22. P. 213–235.
Love O.P., McGowan P.O., Sheriff M.J. Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities // Functional Ecology. 2013. V. 27(1). P. 81–92.
Lukowiak K., Sunada H., Teskey M., Dalesman S. Environmentally relevant stressors alter memory formation in the pond snail Lymnaea // J. Experimental Biology. 2014. V. 217. P. 76–83.
Marshall D., Uller T. When is a maternal effect adaptive? // Oikos. 2007. V. 116(12). P. 1957–1963.
Meshcheryakov V.N. The common pond snail Lymnaea stagnalis //Animal species for developmental studies. – Springer, Boston, MA, 1990. P. 69–132.
Moore M.P., Whiteman H.H., Martin R.A. A mother’s legacy: the strength of maternal effects in animal populations // Ecology Letters. 2019. V. 22(10). P. 1620–1628.
Sheriff M.J., Bell A., Boonstra R., Dantzer B., Lavergne S.G., McGhee K.E., MacLeod K.J., Winandy L., Zimmer C., Love O.P. Integrating ecological and evolutionary context in the study of maternal stress. Integrative and comparative biology. 2017. V. 57(3). P. 437–449.
Sheriff M.J., Love O.P. Determining the adaptive potential of maternal stress // Ecology letters. 2013. V. 16(2). V. 271–280.
van der Steen W., Jager J.C., Tiemersma D. The influence of food quantity on feeding, reproduction, and growth in the pond snail Lymnaea stagnalis (L.) with some methodological comments // Proc. K. Ned. Akad. Wet. 1973. V. 76. P. 47–60.