Experimental simulation of environmental warming selects against pigmented morphs of land snails.

Heinz‐R Köhler,Henri A Thomassen,Silvia Mazzuca,Mark C Bilton,Christophe Mazzia,Janne K Y Burmester,Josep Florit Gomila,Gregorio Moreno‐Rueda,Lilith Sawallich,Luis J Chueca,Line Capowiez,Josep Quintana Cardona,Giuseppe Manganelli,Rita Triebskorn,Amalia Piro,Katharina Peschke,Yvan Capowiez,Nils Kaczmarek,Leonardo Favilli,Αλεξάνδρα Στάικου ,Heiner Eckstein

doi:10.1002/ece3.7002

Abstract

In terrestrial snails, thermal selection acts on shell coloration. However, the biological relevance of small differences in the intensity of shell pigmentation and the associated thermodynamic, physiological, and evolutionary consequences for snail diversity within the course of environmental warming are still insufficiently understood. To relate temperature‐driven internal heating, protein and membrane integrity impairment, escape behavior, place of residence selection, water loss, and mortality, we used experimentally warmed open‐top chambers and field observations with a total of >11,000 naturally or experimentally colored individuals of the highly polymorphic species Theba pisana (O.F. MÜller, 1774). We show that solar radiation in their natural Mediterranean habitat in Southern France poses intensifying thermal stress on increasingly pigmented snails that cannot be compensated for by behavioral responses. Individuals of all morphs acted neither jointly nor actively competed in climbing behavior, but acted similarly regardless of neighbor pigmentation intensity. Consequently, dark morphs progressively suffered from high internal temperatures, oxidative stress, and a breakdown of the chaperone system. Concomitant with increasing water loss, mortality increased with more intense pigmentation under simulated global warming conditions. In parallel with an increase in mean ambient temperature of 1.34°C over the past 30 years, the mortality rate of pigmented individuals in the field is, currently, about 50% higher than that of white morphs. A further increase of 1.12°C, as experimentally simulated in our study, would elevate this rate by another 26%. For 34 T. pisana populations from locations that are up to 2.7°C warmer than our experimental site, we show that both the frequency of pigmented morphs and overall pigmentation intensity decrease with an increase in average summer temperatures. We therefore predict a continuing strong decline in the frequency of pigmented morphs and a decrease in overall pigmentation intensity with ongoing global change in areas with strong solar radiation.

Highlights

To better understand and predict the impact of climate warming on organisms requires multitrait approaches (Debecker & Stoks, 2019)
Among the best-studied examples for phenotypic variation in response to climate and habitat are shell pigmentation polymorphisms of helicoid land snails, which have been investigated in detail for more than 50 years
The manifold results and conclusions of these studies suggest that the role of thermal selection in the evolutionary ecology of land snails in response to global change, and its relevance for differently pigmented morphs, remains only partly understood

Summary

| INTRODUCTION

To better understand and predict the impact of climate warming on organisms requires multitrait approaches (Debecker & Stoks, 2019). Changes in pigmentation intensity were interpreted to result from temporal and spatial variation in the strength and direction of selection (Cook, 2005; Johnson, 2011, 2012) or from epigenetic nondirectional changes within the limits of phenotypic plasticity (Köhler et al, 2009, 2013) Despite their unquestionable importance, none of these studies comprised experimentally modified field conditions or measured physiological or biochemical parameters that could have helped to mechanistically understand thermal stress-exerted selection pressure. The manifold results and conclusions of these studies suggest that the role of thermal selection in the evolutionary ecology of land snails in response to global change, and its relevance for differently pigmented morphs, remains only partly understood This is especially true in snails with extremely variable shell coloration such as the Mediterranean species T. pisana. We tested our predictions by field observations on morph frequencies in other Mediterranean sites that already are subject to such thermal conditions that are expected for the experimental site

| MATERIALS AND METHODS

Findings

| DISCUSSION