Abstract

BackgroundExtreme environments can impose strong ecological and evolutionary pressures at a local level. Ectotherms are particularly sensitive to low-temperature environments, which can result in a reduced activity period, slowed physiological processes and increased exposure to sub-zero temperatures. The aim of this study was to assess the behavioural and physiological responses that facilitate survival in low-temperature environments. In particular, we asked: 1) do high-altitude common frog (Rana temporaria) adults extend the time available for larval growth by breeding at lower temperatures than low-altitude individuals?; and 2) do tadpoles sampled from high-altitude sites differ physiologically from those from low-altitude sites, in terms of routine metabolic rate (RMR) and freeze tolerance? Breeding date was assessed as the first day of spawn observation and local temperature recorded for five, paired high- and low-altitude R. temporaria breeding sites in Scotland. Spawn was collected and tadpoles raised in a common laboratory environment, where RMR was measured as oxygen consumed using a closed respiratory tube system. Freeze tolerance was measured as survival following slow cooling to the point when all container water had frozen.ResultsWe found that breeding did not occur below 5°C at any site and there was no significant relationship between breeding temperature and altitude, leading to a delay in spawning of five days for every 100 m increase in altitude. The relationship between altitude and RMR varied by mountain but was lower for individuals sampled from high- than low-altitude sites within the three mountains with the highest high-altitude sites (≥900 m). In contrast, individuals sampled from low-altitudes survived freezing significantly better than those from high-altitudes, across all mountains.ConclusionsOur results suggest that adults at high-altitude do not show behavioural adaptations in terms of breeding at lower temperatures. However, tadpoles appear to have the potential to adapt physiologically to surviving at high-altitude via reduced RMR but without an increase in freeze tolerance. Therefore, survival at high-altitude may be facilitated by physiological mechanisms that permit faster growth rates, allowing completion of larval development within a shorter time period, alleviating the need for adaptations that extend the time available for larval growth.

Highlights

  • Extreme environments can impose strong ecological and evolutionary pressures at a local level

  • We have previously shown that local adaptation to high-altitude environments occurs even in the face of high gene flow, suggesting that temperature exerts a strong selective pressure [45]

  • This study answers the questions: 1) do high-altitude adults extend the time available for larval growth by breeding at lower temperatures than low-altitude individuals?; and 2) do tadpoles sampled from high-altitude sites differ physiologically from those from low-altitude sites, in terms of routine metabolic rate and freeze tolerance?

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Summary

Introduction

Extreme environments can impose strong ecological and evolutionary pressures at a local level. Ectotherms are sensitive to low-temperature environments, which can result in a reduced activity period, slowed physiological processes and increased exposure to sub-zero temperatures. We asked: 1) do high-altitude common frog (Rana temporaria) adults extend the time available for larval growth by breeding at lower temperatures than low-altitude individuals?; and 2) do tadpoles sampled from high-altitude sites differ physiologically from those from low-altitude sites, in terms of routine metabolic rate (RMR) and freeze tolerance? Plastic and adaptive responses to low temperature environments have been widely recorded (for a review see [8]) and can result in cryptic divergence between populations inhabiting different temperature regimes (counter-gradient variation; [9]). Reduced activity periods in low-temperature environments, in combination with low-temperature driven growth-rate reductions, can result in lower sizes at important lifehistory events such as metamorphosis and reproduction [13]. Smaller sizes can translate to lower fitness when weight is positively correlated with survival or reproductive success [13,14]

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