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Excoffier, L.

Publications and source records attributed to Excoffier, L..

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Genomic analysis of fast expanding bacteria reveals new molecular adaptive mechanisms

Bacterial populations have been shown to accumulate deleterious mutations during spatial expansions that overall decrease their fitness and ability to grow. However, it is unclear if and how they can respond to selection in face of this mutation load. We examine here if artificial selection can counteract the negative effects of range expansions. We investigated the molecular evolution of 20 lines (SEL) selected for fast expansions and compared them to 20 lines without artificial selection (CONTROL). We find that all 20 SEL lines have been able to increase their expansion speed relative to the ancestral line, unlike CONTROL lines, showing that enough beneficial mutations are produced during spatial expansions to counteract the negative effect of expansion load. Importantly, SEL and CONTROL lines have similar numbers of mutations indicating that they evolved for the same number of generations and that increased fitness is not due to a purging of deleterious mutations. We find that loss of function (LOF) mutations are better at explaining the increased expansion speed of SEL lines than non-synonymous mutations or a combination of the two. Interestingly, most LOF mutations are found in simple sequence repeats located in genes involved in gene regulation and gene expression. We postulate that such potentially reversible mutations could play a major role in the rapid adaptation of bacteria to changing environmental conditions by shutting down expensive genes and adjusting gene expression.\n\nAuthor SummaryWe investigated if strong artificial selection for fast expansion can counteract the negative effects of range expansion which had been shown to lead to an accumulation of deleterious mutations. This experiments showed that i) an increase in expansion speed could occur if bacteria were selected from the largest protruding sectors, and ii) that artificially selected bacterial lines accumulated about the same number of mutations than simply expanding line suggesting that the observed increased fitness is not due to increased purifying selection where deleterious mutations would have been removed in fast growing lines. We find that loss of function (LOF) mutations are best explaining the observed increased expansion speed in selected lines. These mutations, which are known to play an important role in adaptive processes in bacterial populations, frequently consist in small insertion-deletions in simple sequence repeats, and are thus relatively easily reversible. They could thus act as switches that can reversibly shut down genes. Our results therefore suggest that shutting down expensive genes and adjusting gene expression are important for adaptive processes during range expansion.

evolutionary biology

Mutation load dynamics during environmentally-driven range shifts

The fitness of spatially expanding species has been shown to decrease over time and space, but specialist species tracking their changing environment and shifting their range accordingly have been little studied. We use individual-based simulations and analytical modeling to compare the impact of range expansions and range shifts on genetic diversity and fitness loss, as well as the ability to recover fitness after either a shift or expansion. We find that the speed of a shift has a strong impact on fitness evolution. Fastest shifts show the strongest fitness loss per generation, but intermediate shift speeds lead to the strongest fitness loss per geographic distance. Range shifting species lose fitness more slowly through time than expanding species, however, their fitness compared at equivalent geographic distances spread can be considerably lower. These counter-intuitive results arise from the combination of time over which selection acts and mutations enter the system. Range shifts also exhibit reduced fitness recovery after a geographic shift and may result in extinction, whereas range expansions can persist from the core of the species range. The complexity of range expansions and range shifts highlights the potential for severe consequences of environmental change on species survival.\n\nAuthor SummaryAs environments change through time across the globe, species must adapt or relocate to survive. Specialized species must track the specific moving environments to which they are adapted, as compared to generalists which can spread widely. During colonization of new habitat, individuals can accumulate deleterious alleles through repeated bottlenecks. We show through simulation and analytic modeling that the process by which these alleles accumulate changes depending upon the speed at which populations spread over a landscape. This is due to the increased efficacy of selection against deleterious variants at slow speeds of range shifts and decreased input of mutations at faster speeds of range shifts. Under some selective circumstances, shifting of a species range leads to extinction of the entire population. This suggests that the rate of environmental change across the globe will play a large role in the survival of specialist species as compared to more generalist species.

evolutionary biology

The evolutionary history of Nebraska deer mice: local adaptation in the face of strong gene flow

The interplay of gene flow, genetic drift, and local selective pressure is a dynamic process that has been well studied from a theoretical perspective over the last century. Wright and Haldane laid the foundation for expectations under an island-continent model, demonstrating that an island-specific beneficial allele may be maintained locally if the selection coefficient is larger than the rate of migration of the ancestral allele from the continent. Subsequent extensions of this model have provided considerably more insight. Yet, connecting theoretical results with empirical data has proven challenging, owing to a lack of information on the relationship between genotype, phenotype, and fitness. Here, we examine the demographic and selective history of deer mice in and around the Nebraska Sand Hills, a system in which variation at the Agouti locus affects cryptic coloration that in turn affects the survival of mice in their local habitat. We first genotyped 250 individuals from eleven sites along a transect spanning the Sand Hills at 660,000 SNPs across the genome. Using these genomic data, we found that deer mice first colonized the Sand Hills following the last glacial period. Subsequent high rates of gene flow have served to homogenize the majority of the genome between populations on and off the Sand Hills, with the exception of the Agouti pigmentation locus. Furthermore, mutations at this locus are strongly associated with the pigment traits that are strongly correlated with local soil coloration and thus responsible for cryptic coloration.

evolutionary biology

Detecting Gene Subnetworks Under Selection In Biological Pathways

Advances in high throughput sequencing technologies have created a gap between data production and functional data analysis. Indeed, phenotypes result from interactions between numerous genes, but traditional methods treat loci independently, missing important knowledge brought by network-level emerging properties. Therefore, evidencing selection acting on multiple genes affecting the evolution of complex traits remains challenging. In this context, gene network analysis provides a powerful framework to study the evolution of adaptive traits and facilitates the interpretation of genome-wide data. To tackle this problem, we developed a method to analyse gene networks that is suitable to evidence polygenic selection. The general idea is to search biological pathways for subnetworks of genes that directly interact with each other and that present unusual evolutionary features. Subnetwork search is a typical combinatorial optimization problem that we solve using a simulated annealing approach. We have applied our methodology to find signals of adaptation to high-altitude in human populations. We show that this adaptation has a clear polygenic basis and is influenced by many genetic components. Our approach improves on classical tests for selection based on single genes by identifying both new candidate genes and new biological processes involved in adaptation to altitude.

bioinformatics

Accumulation of deleterious mutations during bacterial range expansions

Recent theory predicts that the fitness of pioneer populations can decline when species expand their range, due to high rates of genetic drift on wave fronts making selection less efficient at purging deleterious variants. To test these predictions, we studied the fate of mutator bacteria expanding their range for 1650 generations on agar plates. In agreement with theory, we find that growth abilities of strains with a high mutation rate (HMR lines) decreased significantly over time, unlike strains with a lower mutation rate (LMR lines) that present 3-4 times fewer mutations. Estimation of the distribution of fitness effect (DFE) under a spatially explicit model reveals a mean negative effect for new mutations (-0.38%), but it suggests that both advantageous and deleterious mutations have accumulated during the experiment. Furthermore, we show that the fitness of HMR lines measured in different environments has decreased relative to the ancestor strain, whereas that of LMR lines remained unchanged. Our results thus suggest that successful expanding species are affected by deleterious mutations that accumulate during the expansion process, leading to a drastic impairment of their evolutionary potential.

evolutionary biology