Thermal traits for reproduction and recruitment differ between Arctic and Atlantic kelp Laminaria digitata.

Neusa Martins,Gareth A. Pearson,Ester A. Serrão,Inka Bartsch,Julien Bernard,Adrian Zwolicki

doi:10.1371/journal.pone.0235388

Neusa Martins, Gareth A. Pearson + Show 4 more

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https://doi.org/10.1371/journal.pone.0235388

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Abstract

The plasticity of different kelp populations to heat stress has seldom been investigated excluding environmental effects due to thermal histories, by raising a generation under common garden conditions. Comparisons of populations in the absence of environmental effects allow unbiased quantification of the meta-population adaptive potential and resolution of population-specific differentiation. Following this approach, we tested the hypothesis that genetically distinct arctic and temperate kelp exhibit different thermal phenotypes, by comparing the capacity of their microscopic life stages to recover from elevated temperatures. Gametophytes of Laminaria digitata (Arctic and North Sea) grown at 15°C for 3 years were subjected to common garden conditions with static or dynamic (i.e., gradual) thermal treatments ranging between 15 and 25°C and also to darkness. Gametophyte growth and survival during thermal stress conditions, and subsequent sporophyte recruitment at two recovery temperatures (5 and 15°C), were investigated. Population-specific responses were apparent; North Sea gametophytes exhibited higher growth rates and greater sporophyte recruitment than those from the Arctic when recovering from high temperatures, revealing differential thermal adaptation. All gametophytes performed poorly after recovery from a static 8-day exposure at 22.5°C compared to the response under a dynamic thermal treatment with a peak temperature of 25°C, demonstrating the importance of gradual warming and/or acclimation time in modifying thermal limits. Recovery temperature markedly affected the capacity of gametophytes to reproduce following high temperatures, regardless of the population. Recovery at 5°C resulted in higher sporophyte production following a 15°C and 20°C static exposure, whereas recovery at 15°C was better for gametophyte exposures to static 22.5°C or dynamic heat stress to 25°C. The subtle performance differences between populations originating from sites with contrasting local in situ temperatures support our hypothesis that their thermal plasticity has diverged over evolutionary time scales.

Highlights

Thermal adaptation studies have recently focused widely on anthropogenically induced climate change in terms of the consequences of shifts in mean temperatures [1, 2]
Distinguishing genetic and phenotypic variation among populations within a species is rare, as intraspecific acclimation versus adaptation along distributional ranges are difficult to disentangle, requiring common garden conditions to verify if a generation of individuals that develop from meiospores/zygotes in the same conditions still retained different ecophysiological responses to the same thermal extremes
Vegetative cultures were maintained at 15 ̊C under 3 μmol photons m-2 s-1 of red light (LED Mitras daylight 150 controlled by ProfiLux 3, GHL Advanced Technology, Kaiserslautern, Germany), 16:8 h light:dark (LD) cycle in sterile full strength Provasoli enriched seawater (PES; Provasoli [40], modifications: HEPES buffer instead of TRIS, double concentration of Na2glycerophosphate) until the start of the experiment

Summary

Introduction

Thermal adaptation studies have recently focused widely on anthropogenically induced climate change in terms of the consequences of shifts in mean temperatures [1, 2]. Adaptive changes among populations may be driven be the extreme thermal values experienced, such as the frequency, intensity and persistence of extreme climatic events [3]. Such complex conditions of environmental change, including the rate and duration of heat spikes, might have important implications for ecophysiological performance [4] and consequent population divergence, but remain insufficiently understood. Distinguishing genetic and phenotypic variation among populations within a species is rare, as intraspecific acclimation versus adaptation along distributional ranges are difficult to disentangle, requiring common garden conditions to verify if a generation of individuals that develop from meiospores/zygotes in the same conditions still retained different ecophysiological responses to the same thermal extremes

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