Population genetics of the common frog (Rana temporaria) in relation to climate

My PhD research focused on how individuals interact with their environment. By using populations of the same species exposed to different environments I was able to relate genotype to phenotype and environmental parameters.

The way that individuals respond and adapt to their environment, either through genetic variation or plasticity, gives us an insight into which factors influence fitness and the strength of the selection. This is especially important when environmental factors are changing, often due to anthropogenic pressures. Using knowledge of current interactions between individuals and their environment allows us to make more accurate predictions about responses to a change in that environment, leading to creation of knowledge- based action plans and conservation strategies.

Altitudinal gradients show rapid changes in environmental factors, such as temperature, even over short geographical distances. Therefore, mountains offer the ideal opportunity to assess how the environment has influenced genotype and phenotype within a species. The common frog, Rana temporaria, occurs from sea level to over a 1000m at the top of Scotland’s highest mountains. Looking at whether, and in what way, populations of the common frog have adapted to the different temperature regimes along an altitudinal gradient allowed me to make predictions about how they will be affected by ongoing climate change.

Findings

The overall aim of this research was to assess population-level relationships with climate using Rana temporaria in Scotland, in order to make predictions about susceptibility to environmental change. We assessed fine-scale population structure in relation to current climatic conditions along altitudinal gradients. No population structure was found using microsatellites within or between altitudinal gradients at any scale (3-50km), despite a mean annual temperature difference of 4.5°C between low- and high- altitude sites. Levels of genetic diversity and heterozygosity were considerable but did not vary by site, altitude or temperature. These results suggested a greater dispersal ability and lower site philopatry of R. temporaria than has been found for other amphibians and that movement of individuals was not limited by different thermal environments.

We then went on to assess whether local adaptation to altitude had taken place in the face of high gene flow and examined the environmental drivers of this local adaptation. We found that R. temporaria showed evidence of local adaptation in all larval fitness traits measured: metamorphic weight, SVL gain, larval period and growth rate. However, only variation in larval period and growth rate was consistent with adaptation to altitude. Moreover, this was only evident in the three highest mountains (high- altitude sites at least 900m), suggesting the possibility of a threshold for local adaptation. This variation was correlated with temperature, suggesting that temperature acts as a strong environmental selection pressure influencing local adaptation along altitudinal gradients, even in the face of high gene flow. Furthermore, by using multiple common temperature treatments to assess local adaptation, I was able to look at genotype-by-environment interactions and discovered that individuals were phenotypically plastic in terms of all larval traits studied except SVL gain.

Having established that R. temporaria are locally adapted to temperature, we went on to investigate the physiological and behavioural adaptations that allow survival at high-altitude in low-temperature environments. Larval R. temporaria showed reduced routine metabolic rate at high-altitude, but only in the three highest mountains, where increased growth rate had been previously observed. These results suggest that there is a resource-limited trade-off between growth rate and routine metabolic rate in these mountains. High- altitude individuals were not more freeze tolerant than their low-altitude neighbours, and adult R. temporaria did not breed at a lower temperature than low-altitude individuals, suggesting these are not responses linked to survival in low-temperature environments.

Finally, we assessed whether the amphibian egg pathogen, Saprolegnia, varied spatially in terms of presence and species composition. Four species of Saprolegnia were isolated overall, multiple Saprolegnia water moulds were isolated from within sites, and species composition varied between sites. A lower acidity was linked toSaprolegnia presence, but genetic distance between samples was not correlated with environmental or geographic distance. These findings question the previous focus on S. ferax as the primary agent of Saprolegnia infection and suggest that future studies of virulence need to consider the synergistic effect of multiple Saprolegnia species.

Read more about the results of this study here:

Muir, A. P., Biek, R. and Mable, B. K. (2014) Behavioral and physiological adaptations to low-temperature environments in the common frog, Rana temporariaBMC Evolutionary Biology14:110 doi:10.1186/1471-2148-14-110 "highly accessed"

Muir A.P., Biek R., Thomas R. & Mable B.K. (2014) Local adaptation with high gene flow: temperature parameters drive adaptation to altitude in the common frog (Rana temporaria) Molecular Ecology, 23(3), 561-574. Available open access: DOI: 10.1111/mec.12624

Muir A.P., Thomas R., Biek R. & Mable B.K. (2013) Using genetic variation to infer associations with climate in the common frog, Rana temporaria. Molecular Ecology. 22(14), 3737-3751 DOI: 10.1111/mec.12334