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

 

 

The River Gambia National Park lies in the heart of the The Gambia, West Africa, close to the village of Sambel Kunda. During the summers of 2005 and 2006 I spent four months working in The River Gambia National Park as part of research and community based student expeditions. During 2005 I spent time in Sambel Kunda, teaching biodiversity and English at the local school, building a library for the community and being involved with biodiversity research taking place in the national park.

During 2005-2006 I took on the role of expedition leader for the team of eight undergraduates. This involved writing grant proposals, holding fundraising events, ensuring the team attended suitable training events, overseeing project planning and liasing with our contact in The Gambia. During the trip I was responsible for all day to day aspects of running camp, overseeing research and community based projects, managing expedition members and being the first port of call in a crisis.

During 2007 and 2008 I spent a year living, working and researching with the Kichwa community, San José de Payamino, Ecuador. The territory of San José de Payamino consists of 27,000 hectares of primary lowland tropical rainforest in south-eastern Ecuador. The community has formed a conservation and sustainable development partnership, the Payamino Project, with Zoos Go Wild and Aalborg Zoo in Denmark.

Whilst working as a research station manager for the Payamino Project, I also undertook research for my masters thesis looking at the previously unstudied levels of amphibian diversity in the area. Work in remote areas with difficult terrain, high biodiversity and a restricted timeframe can make diversity assessments difficult. Whilst carrying out a standard amphibian species richness assessment using night transects, I also trialled a new rapid assessment technique previously used for birds. The species list technique allows opportunistic encounters to be standardised in terms of effort. This means all available time can be used for recording species without “wasted” data that can’t be used for analysis, whilst still being comparable between sites. The species list technique offers a new efficient rapid assessment technique for tropical rainforest amphibians. For further information please see:

Muir, A.P. & Muir, M.C.A. (2011) A New Rapid Assessment Technique for Amphibians: Introduction of the Species List Technique from San José de Payamino, Ecuador. Herpetological Review, 42, 149- 151. Download a copy

During my time in Ecuador I recorded 64 species of amphibians (see images of some of them here)and saw a host of other biodiversity. I led a student herpetology group from the University of Glasgow during their six week stay, including collecting data for undergraduate theses. I learnt Spanish, the traditions and culture of the Kichwa community and how to live and work in remote environments. My enthusiasm for research and conservation of amphibians was formed during my time here.

Nyctimantis rugiceps

Hypsiboas geographicus

Osteocephalus cabrerai

Edalhorina perezi