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Environmental Stressors Induced Strong Small-Scale Phenotypic bioRxiv preprint doi: https://doi.org/10.1101/2020.10.06.327767; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Environmental stressors induced strong small-scale phenotypic 2 differentiation in a wide-dispersing marine snail 3 Nicolás Bonel1,2,3*, Jean-Pierre Pointier4 & Pilar Alda1,2 4 5 6 1 Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS—CCT—CONICET Bahía 7 Blanca), Camino de la Carrindanga km 7, Bahía Blanca 8000, Argentina. 8 9 10 2 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina. 11 12 13 3 Centre d’Écologie Fonctionnelle et Évolutive, UMR 5175, CNRS—Université de Montpellier, 14 Université Paul-Valéry Montpellier—École Pratique des Hautes Études—IRD, 34293 Montpellier Cedex 15 05, France. 16 17 4 PSL Research University, USR 3278 CNRS–EPHE, CRIOBE Université de Perpignan, Perpignan, 18 France. 19 20 * To whom correspondence should be addressed: [email protected] (N. Bonel) 21 22 23 24 25 Running head: Small-scale phenotypic differentiation in a wide-dispersing snail 26 27 28 29 30 31 Key words: adaptive plasticity, shell characters, genital morphology, intertidal 32 zonation, contrasting selection pressures, planktotrophic snail, high dispersal potential. 33 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.06.327767; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 ABSTRACT 2 Heterogeneous environments pose a particular challenge for organisms because the 3 same phenotype is unlikely to perform best regardless of the types of stress it 4 encounters. To understand how species meet this challenge, we investigated the extent 5 to which contrasting selection pressures induced ecological and phenotypic responses in 6 a natural population of a wide-dispersing marine snail. We analyzed several traits of 7 Heleobia australis (Rissooidea: Cochliopidae) collected from heterogeneous habitats 8 from the intertidal area of the Bahía Blanca estuary, Argentina. We also conducted 9 molecular analyses by amplifying the COI gene in individuals sampled from each 10 habitat. We found that subpopulations of H. australis, inhabiting close to each other and 11 without physical barriers, exhibited a strong phenotypic differentiation in shell 12 characters and body weight in response to environmental stress conditions, crab 13 predation, and parasites. We proved that this differentiation occurred even early in life 14 as most of the characters observed in juveniles mirrored those found in adults. We also 15 found a clear divergence in penis size in snails collected from each habitat and raised in 16 common garden laboratory conditions. The molecular analyses confirmed that the 17 individuals studied constituted a single species despite the strong phenotypic difference 18 among subpopulations. Altogether, the small-scale phenotypic differentiation in this 19 planktotrophic snail can be interpreted as adaptive plasticity responses to directional 20 selection imposed by strong gradients of abiotic and biotic stressors. These findings 21 might contribute to a more complete understanding of the spatial scale at which 22 adaptive differentiation can occur, which has historically been understudied in intertidal 23 species. 24 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.06.327767; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 INTRODUCTION 2 If organisms have difficulties in adapting to human-induced global change and fail to 3 track projected environmental changes, populations become vulnerable to decline and 4 extinction (Hill et al. 2011, Hoffmann & Sgrò 2011). Phenotypic plasticity, a common 5 feature in nature across many taxa, is the ability of a single genotype to express different 6 phenotypes in dissimilar biotic or abiotic environments (Travis 1994, West-Eberhard 7 2003). Many studies indicate a role of plasticity in shaping phenotypic responses as an 8 effective mechanism that can greatly improve the conditions for persistence of 9 populations facing abrupt environmental shift by facilitating rapid adaptation to the new 10 selection pressures (Price et al. 2003, Ghalambor et al. 2007, Chevin & Lande 2009). 11 Adaptive plasticity that places populations close enough to the new favored phenotypic 12 optimum for directional selection to act provides the first step in adaptation to new 13 environments on ecological time scales (see review in Ghalambor et al. 2007). In other 14 words, such plasticity––when operates jointly with directional selection––can facilitate 15 the process of adaptive evolution in a new environment (De Jong 2005, Fusco & Minelli 16 2010, Merilä & Hendry 2014) by which non-heritable environmentally induced 17 variation leads to adaptive heritable variation, the so-called Baldwin Effect, or more 18 commonly known as ‘genetic assimilation’ (reviewed in Waddington 1953, West- 19 Eberhard 1989, Pigliucci et al. 2006; but see West-Eberhard 2003). In this sense, 20 adaptive phenotypic plasticity is crucial for the long-term persistence of populations 21 facing new environmental stress brought about by human-induced global change (Hill et 22 al. 2011). 23 24 Temperate marine habitats, in particular the intertidal zone, exhibit great variability in 25 environmental factors mainly driven by the fall and rise of the tides, creating areas on 26 the shore that are alternately immersed and exposed (Denny & Paine 1998, Bourdeau et 27 al. 2015). The transitional nature of the intertidal habitat from marine to terrestrial 28 conditions strongly influences the physiology and the ecology of intertidal organisms 29 due to the increase in environmental harshness (e.g. desiccation, extremes in 30 temperature and salinity) along the vertical zonation of the intertidal area (Vermeij 31 1972, Denny & Paine 1998, Mouritsen et al. 2018). From this perspective, intertidal 32 organisms, such as aquatic gastropods, are likely to exhibit increased adaptive 33 phenotypic plasticity in response to such environmental selective pressures (Berrigan & 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.06.327767; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Scheiner 2004). Despite the intertidal area spans a strong selective gradient, small-scale 2 phenotypic divergence and adaption of intertidal organisms has been underestimated 3 (Hays 2007; see also review by Sanford & Kelly 2011). 4 5 Phenotypic variation in shell traits is particularly widespread in gastropods (Bourdeau et 6 al. 2015) and their shells offer an easily measured and permanent record of how the 7 organism responded to local abiotic (e.g. water chemistry, temperature) and biotic (e.g. 8 predation, parasitism) agents (Dillon et al. 2013). Major environmental factors as 9 prolonged submersion times, desiccation, high temperature, and extreme salinity across 10 the vertical zonation create contrasting selective pressures that give rise to opposite shell 11 trait responses (Struhsaker 1968, Johannesson & Johannesson 1996). For instance, 12 prolonged submersion times enhance foraging times and the absorption of calcium 13 carbonate from water leading to higher shell growth rates, which result in larger and 14 narrower shells and increased body mass (Vermeij 1973, review by Chapman 1995). By 15 contrast, snails from upper intertidal habitats that are periodically exposed to hot and 16 dry conditions and have only a limited time each day to feed exhibit the opposite shell 17 and body mass responses and are characterized by having a smaller aperture size, which 18 has been correlated to an increase in resistance to high desiccation in upper intertidal 19 habitats (Machin 1967, Vermeij 1973, Chapman 1995, Melatunan et al. 2013, 20 Schweizer et al. 2019). 21 22 Predators are one component of the heterogeneity across the intertidal zone because 23 they are often distributed patchily in time and space creating a steep selection gradient 24 in predation risk, which, in turns, can promote an adaptive evolutionary shell response 25 (Boulding & Hay 1993, Bourdeau 2011). Predator-induced plasticity primarily linked to 26 shell defenses are not limited to shell thickening (more resistant to crushing) as snails 27 are capable of plastically altering different aspects of their shell shape (i.e. increased 28 globosity; lower shell length to width ratio) or aperture (i.e. more elongated; higher 29 aperture length to width ratio), which prevents the crab from pulling the soft parts out of 30 the shell (Johannesson 2003, Dillon et al. 2013, Bourdeau et al. 2015). However, not all 31 phenotypic plasticity triggered by environmental conditions is adaptive (Ghalambor et 32 al. 2007). Some plastic trait responses, usually those imposed by the biochemistry and 33 physiology of the organism, can be reversed over short time scales, which is not the 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.10.06.327767; this version posted March 11, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder.
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