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

Muir, Anna Patricia (2013) Population genetics of the common frog (Rana temporaria) in relation to climate. PhD thesis, University of Glasgow.

Abstract

Ecological responses to a changing climate have been well documented in a broad range of species, predominantly in terms of range movements and phenological changes. When faced with a changing environment, species survival will depend on the ability to: 1) evade changes in climate, via dispersal; 2) evolve, via natural selection; and/or 3) plastically change their phenotype, without underlying genetic changes. The potential for an organism to evade, evolve or plastically respond to a changing environment can be predicted by inferring relationships with current climatic conditions. Altitudinal gradients have been proposed as being particularly suitable for environmental change studies due to the rapid variation in climate even over short geographical distances. Species that inhabit altitudinal gradients experience a range of climatic conditions across their range and are thus subject to varying selection pressures. Changes in temperature are predicted to particularly influence ectotherms due to the direct effect on physiological processes. The common frog (Rana temporaria) occurs from zero to over a thousand metres along altitudinal gradients in Scotland, offering the opportunity to assess the influence of temperature on organism responses. The overall aim of this thesis was to assess population-level relationships with climate, in order to make predictions regarding susceptibility to a changing climate, focussing on R. temporaria in Scotland. In Chapter 2, I inferred colonisation patterns within Europe following the last glacial maximum by combining new and previously compiled mitochondrial cytochrome b DNA sequences. I found that the mitochondrial DNA sequences from my Scottish samples were identical to, or clustered with, the common haplotype previously identified from Western Europe. This clade showed very low mitochondrial genetic variation, consistent with a leptokurtic model of range expansion, where low numbers of long-distance dispersers cause multiple founder events. Second, I assessed fine-scale genetic variation in relation to current temperature gradients using microsatellites. No population structure was found within or between altitudinal gradients at any scale (3-50km; average FST= 0.02), 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. In Chapter 3, common temperature treatments were used to assess phenotypic differentiation and phenotypic plasticity variation in relation to altitude in terms of larval fitness traits. Local adaptation to altitude was assessed using QST-FST analyses and adaptive phenotypic divergence was then related to environmental parameters using Mantel tests, to look for drivers of selection. I found that R. temporaria showed evidence of local adaptation in all larval fitness traits measured. However, only variation in larval period and growth rate was consistent with adaptation to altitude. Moreover, this was only evident in the three mountains with the highest high-altitude sites (at least 900m). Adaptive divergence in traits that were locally adapted to altitude was correlated with spring temperature, suggesting that temperature acts as a strong environmental selection pressure influencing local adaptation even in the face of high gene flow. In Chapter 4, the physiological and behavioural responses that facilitate survival in high-altitude environments were evaluated, in terms of routine metabolic rate and freeze tolerance in tadpoles, and breeding temperature in adults. I found that routine metabolic rate was lower for individuals sampled from high- than low-altitude sites but only from the three mountains with the highest high-altitude sites (at least 900m). Glucose accumulation during freezing was not significantly different based on altitude. However, individuals from low-altitude survived freezing significantly better than those from high-altitude, across all mountains. Breeding did not occur below 5˚C at any site and there was no significant difference in breeding temperature between high- and low-altitude sites, leading to high-altitude individuals spawning 30 days later than those at low-altitude. My results suggest that tadpoles are adapted physiologically to surviving at high-altitude via reduced routine metabolic rate, but only at the highest breeding sites. Finally, in Chapter 5, I assessed the spatial variation in species presence and composition of parasitic water moulds in the genus Saprolegnia found on R. temporaria eggs. Thirteen samples isolated from four sites were identified as members of the Saprolegniaceae. Four putative species of Saprolegnia were isolated overall, multiple Saprolegnia water moulds were isolated from within sites, and species composition varied between sites. Acidity was significantly lower at sites where
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Saprolegniaceae were present, 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 in amphibians and suggest that future studies of virulence need to consider the synergistic effect of multiple Saprolegnia species. In conclusion, R. temporaria show the potential for evasion, evolution and plastic responses to a changing climate and my results suggest that the outlook is positive for survival of the common frog in Scotland.

• Item Type: Thesis (PhD)
• Qualification Level: Doctoral
• Keywords: Population genetics, climate change, amphibian, altitude, local adaptation, phenotypic plasticity, Saprolegnia
• Subjects: Q Science > QL Zoology
• Colleges/Schools: College of Medical Veterinary and Life Sciences > Institute of Biodiversity Animal Health and Comparative Medicine
• Supervisor's Name: Mable, Dr. Barbara, Biek, Dr. Roman and Thomas, Mr. Rob
• Date of Award: 2013
• Depositing User: Anna Patricia Muir
• Unique ID: glathesis:2013-3858
• Copyright: Copyright of this thesis is held by the author.
• Date Deposited: 06 Feb 2013 09:46
• Last Modified: 25 Jan 2016 14:22
• URI: https://theses.gla.ac.uk/id/eprint/3858