Final Report Summary - INVASIVOLE (Genetics of an invasive species and its parasites: the bank vole in Ireland)
Populations expanding their ranges are often thought to be under strong selection for evolution of specific life-history traits. Theoretical simulation work, supported by empirical studies, suggests that individuals at the wave front of an expanding range should allocate more resources to reproduction and dispersal, leading to accelerating rates of range expansion over time. For example, in Australia, cane toads (Rhinella marinus) at the front of the expanding invasive population show evidence of increased reproductive effort and increased dispersal compared to individuals in previously colonized areas. Species may also lose parasites as they expand their ranges, so increased investment in reproduction and dispersal may be traded-off against reduced investment in immunity. However, range expansions are also predicted to cause a reduction in genetic diversity due to strong genetic drift and founder events at the wave front. Is it possible for adaptation to occur in spite of reduced genetic diversity? Genetic drift and 'allele surfing' can also generate genetic patterns similar to those expected under natural selection. How then can the signal of natural selection be detected genetically?
The bank vole (Myodes glareolus, formerly Clethrionomys glareolus) is a small rodent, found through much of Eurasia, from northern Scandinavia to the Mediterranean and from Siberia to Spain. It was first recorded on Ireland in 1964, in County Limerick in the south-west of the country. Although there had been plenty of field-based studies on Irish small mammals prior to this time, voles had not previously been detected. The bank vole is continuing to expand its range in Ireland, and the process of invasion is not being modified by an eradication program. The bank vole in Ireland can therefore be considered an excellent model system for the study of evolution during range expansions.
The aim of the INVASIVOLE project was to reconstruct the invasion history of the bank vole, to assess patterns of genetic diversity across the range expansion, and to determine whether there is any genetic evidence of adaptation to the range expansion process. In 2010 and 2011, two field campaigns were undertaken to sample bank voles in Ireland. As genetic effects may be restricted to the wave front of the population expansion, the current limits of the bank vole range were determined first. Using knowledge from the first field campaign and data from three previous systematic surveys of the bank vole distribution in Ireland, we estimated the rate of range expansion. We found the rate of expansion to be constant over time, at approximately 2.5 km yr-1. This rate was in very good agreement with that predicted using a reaction-diffusion model parameterized with bank vole life history and dispersal data taken from the literature. These analyses further allowed projections as to when the invasion will likely cover Ireland completely based on the current expansion rate. These results have been published in the journal Biological Invasions (White et al. 2012, Vol. 14, 2203–2215; see publication list).
Having found the current limits of the bank vole range expansion, voles from 14 sample sites were sampled in the following field campaign, arranged in three transects running from the site of introduction to the wave front of the ongoing expansion. Genomic DNA was extracted from all 281 individuals sampled along the transects, and sample material was preserved for further analyses of parasites and morphology. During the outgoing phase of the project at Cornell University Genotyping by Sequencing (GBS), a novel genomic technique developed at Cornell, was used to genotype all the bank voles at 5,979 Single Nucleotide Polymorphism (SNP) loci. 266 of these SNP loci could be localized to genic regions with comparative bioinformatics analyses. We found significant declines in genetic diversity along all three sampling transects, the slope of which did not vary between different classes of SNPs (i.e. genic vs. non-genic). We looked for outlier loci with significant correlations between allele frequency and distance from the introduction site, where the direction of the correlation was the same in all three transects. Amongst these outliers, we found significant enrichment for genic and non-synonymous (mutations that have the potential to affect gene function) SNPs, suggesting the action of selection. Candidates for selection included several genes that could influence behavior and several genes with immunological functions. These results have been published in the journal Molecular Ecology (White et al. 2013, Vol. 22, 2971-2985, see publication list).
Further analytical work on this system is ongoing. These investigations include geometric morphometric analysis of vole skulls to determine whether voles sampled towards the wave-front of the expansion might suffer reduced fitness (assessed as the degree of asymmetry in the skull) due to their reduced genetic diversity. Preliminary data from a subset of skulls suggest sufficient morphological variation in the system for these analyses. In addition, parasites have been collected and identified from the guts and lungs of the 281 sampled voles. In due course, these data will be analyzed to determine the relationships between genetic diversity, demographics and parasite load during the range expansion. The theoretical underpinnings for this work have been discussed in a review paper published in the journal Functional Ecology (White & Perkins 2012, Vol. 26, 1313-1323, see publication list).
Invasive species have negative economic impacts all over the world, including the countries of the European Union. It is very important that research is carried out on all aspects of invasion, including genetics and invasion dynamics. The genetic and evolutionary consequences of range expansion are not only important for species that are currently invasive. Many, if not most, species have recently experienced range expansions. Studies such as undertaken in the course of this project therefore provide much needed fundamental data on processes that affect a wide range of biological systems. They should also prove very useful to wildlife managers, both for conservation of native biodiversity and control of spreading non-indigenous or pest species.
The bank vole (Myodes glareolus, formerly Clethrionomys glareolus) is a small rodent, found through much of Eurasia, from northern Scandinavia to the Mediterranean and from Siberia to Spain. It was first recorded on Ireland in 1964, in County Limerick in the south-west of the country. Although there had been plenty of field-based studies on Irish small mammals prior to this time, voles had not previously been detected. The bank vole is continuing to expand its range in Ireland, and the process of invasion is not being modified by an eradication program. The bank vole in Ireland can therefore be considered an excellent model system for the study of evolution during range expansions.
The aim of the INVASIVOLE project was to reconstruct the invasion history of the bank vole, to assess patterns of genetic diversity across the range expansion, and to determine whether there is any genetic evidence of adaptation to the range expansion process. In 2010 and 2011, two field campaigns were undertaken to sample bank voles in Ireland. As genetic effects may be restricted to the wave front of the population expansion, the current limits of the bank vole range were determined first. Using knowledge from the first field campaign and data from three previous systematic surveys of the bank vole distribution in Ireland, we estimated the rate of range expansion. We found the rate of expansion to be constant over time, at approximately 2.5 km yr-1. This rate was in very good agreement with that predicted using a reaction-diffusion model parameterized with bank vole life history and dispersal data taken from the literature. These analyses further allowed projections as to when the invasion will likely cover Ireland completely based on the current expansion rate. These results have been published in the journal Biological Invasions (White et al. 2012, Vol. 14, 2203–2215; see publication list).
Having found the current limits of the bank vole range expansion, voles from 14 sample sites were sampled in the following field campaign, arranged in three transects running from the site of introduction to the wave front of the ongoing expansion. Genomic DNA was extracted from all 281 individuals sampled along the transects, and sample material was preserved for further analyses of parasites and morphology. During the outgoing phase of the project at Cornell University Genotyping by Sequencing (GBS), a novel genomic technique developed at Cornell, was used to genotype all the bank voles at 5,979 Single Nucleotide Polymorphism (SNP) loci. 266 of these SNP loci could be localized to genic regions with comparative bioinformatics analyses. We found significant declines in genetic diversity along all three sampling transects, the slope of which did not vary between different classes of SNPs (i.e. genic vs. non-genic). We looked for outlier loci with significant correlations between allele frequency and distance from the introduction site, where the direction of the correlation was the same in all three transects. Amongst these outliers, we found significant enrichment for genic and non-synonymous (mutations that have the potential to affect gene function) SNPs, suggesting the action of selection. Candidates for selection included several genes that could influence behavior and several genes with immunological functions. These results have been published in the journal Molecular Ecology (White et al. 2013, Vol. 22, 2971-2985, see publication list).
Further analytical work on this system is ongoing. These investigations include geometric morphometric analysis of vole skulls to determine whether voles sampled towards the wave-front of the expansion might suffer reduced fitness (assessed as the degree of asymmetry in the skull) due to their reduced genetic diversity. Preliminary data from a subset of skulls suggest sufficient morphological variation in the system for these analyses. In addition, parasites have been collected and identified from the guts and lungs of the 281 sampled voles. In due course, these data will be analyzed to determine the relationships between genetic diversity, demographics and parasite load during the range expansion. The theoretical underpinnings for this work have been discussed in a review paper published in the journal Functional Ecology (White & Perkins 2012, Vol. 26, 1313-1323, see publication list).
Invasive species have negative economic impacts all over the world, including the countries of the European Union. It is very important that research is carried out on all aspects of invasion, including genetics and invasion dynamics. The genetic and evolutionary consequences of range expansion are not only important for species that are currently invasive. Many, if not most, species have recently experienced range expansions. Studies such as undertaken in the course of this project therefore provide much needed fundamental data on processes that affect a wide range of biological systems. They should also prove very useful to wildlife managers, both for conservation of native biodiversity and control of spreading non-indigenous or pest species.