The genomic impact of deleterious mutations in isolation with migration models

Tese de mestrado, Biologia Evolutiva e do Desenvolvimento, Universidade de Lisboa, Faculdade de Ciências, 2019The effects of background selection (BGS), i.e. the effect that purifying selection due to removal of deleterious mutations at given site has on linked neutral sites, is well understood in single population models. For recessive deleterious mutations, heterozygotes can have a higher fitness leading to associative overdominance (AOD). Previous studies suggest that BGS may increase genomic differentiation, misleading genomic scans that rely on high differentiation regions to detect genes involved in local adaptation. However, little is known about the interaction of BGS and AOD with gene flow. To characterize the genomic impact of BGS, AOD and migration we used a forward-in-time simulator implemented in the program SLiM 3.2. We considered an isolation with migration model with two populations of constant size. To understand the relative impact of each parameter we used various combinations of migration rates, recombination rates, selective coefficients and dominance coefficients. We find that, in relation to neutral expectations, co-dominant deleterious mutations decrease within population diversity and increase genetic differentiation (FST) between populations, although with high migration (2Nem>10) FST does not deviate from neutral expectation. Consistent with the effect of AOD, for recessive deleterious mutations we found an increase of neutral diversity for selective coefficients s between 0.0001 and 0.1, when recombination rate is lower than the mutation rate. AOD also leads to a decrease in population differentiation (FST), with higher migration rates decreasing the magnitude of this effect. Thus, BGS and AOD can lead to heterogeneous genomic patterns and bias the detection of divergent selection

Maximum likelihood implementation of an isolation-with-migration model for three species

We develop a maximum likelihood (ML) method for estimating migration rates between species using genomic sequence data. A species tree is used to accommodate the phylogenetic relationships among three species, allowing for migration between the two sister species, while the third species is used as an outgroup. A Markov chain characterization of the genealogical process of coalescence and migration is used to integrate out the migration histories at each locus analytically, while Gaussian quadrature is used to integrate over the coalescent times on each genealogical tree numerically. This is an extension of our early implementation of the symmetrical isolation-with-migration model for three species to accommodate arbitrary loci with two or three sequences per locus and to allow asymmetrical migration rates. Our implementation can accommodate tens of thousands of loci, making it feasible to analyze genome-scale datasets to test for gene flow. We calculate the posterior probabilities of gene trees at individual loci to identify genomic regions that are likely to have been transferred between species due to gene flow. We conduct a simulation study to examine the statistical properties of the likelihood ratio test for gene flow between the two ingroup species and of the maximum likelihood estimates of model parameters such as the migration rate. Inclusion of data from a third outgroup species is found to increase dramatically the power of the test and the precision of parameter estimation. We compiled and analyzed several genomic datasets from the Drosophila fruit flies. Our analyses suggest no migration from D. melanogaster to D. simulans, and a significant amount of gene flow from D. simulans to D. melanogaster, at the rate of ~0.02 migrant individuals per generation. We discuss the utility of the multispecies coalescent model for species tree estimation, accounting for incomplete lineage sorting and migration

Ancestral population genomics

The full genomes of several closely related species are now available, opening an emerging field of investigation borrowing both from population genetics and phylogenetics. Providing we can properly model sequence evolution within populations undergoing speciation events, this resource enables us to estimate key population genetics parameters, such as ancestral population sizes and split times. Furthermore, we can enhance our understanding of the recombination process and investigate various selective forces. We discuss the basic speciation models for closely related species, including the isolation and isolation-with-migration models. A major point in our discussion is that only a few complete genomes contain much information about the whole population. The reason being that recombination unlinks genomic regions, and therefore a few genomes contain many segments with distinct histories. The challenge of population genomics is to decode this mosaic of histories in order to infer scenarios of demography and selection. We survey different approaches for understanding ancestral species from analyses of genomic data from closely related species. In particular, we emphasize core assumptions and working hypothesis. Finally, we discuss computational and statistical challenges that arise in the analysis of population genomics data sets

Evolutionary and demographic correlates of Pleistocene coastline changes in the Sicilian wall lizard Podarcis wagleriana

Aim Emergence of coastal lowlands during Pleistocene ice ages might have provided conditions for glacial expansions (demographic and spatial), rather than contraction, of coastal populations of temperate species. Here, we tested these predictions in the insular endemic Sicilian wall lizard Podarcis wagleriana. Location Sicily and neighbouring islands. Methods We sampled 179 individuals from 45 localities across the whole range of P. wagleriana. We investigated demographic and spatial variations through time using Bayesian coalescent models (Bayesian phylogeographic reconstruction, Extended Bayesian Skyline plots, Isolation‐with‐migration models) based on multilocus DNA sequence data. We used species distribution modelling to reconstruct present and past habitat suitability. Results We found two main lineages distributed in the east and west portions of the current species range and a third lineage restricted to a small area in the north of Sicily. Multiple lines of evidence from palaeogeographic (shorelines), palaeoclimatic (species distribution models), and multilocus genetic data (demographic and spatial Bayesian reconstructions) indicate that these lineages originated in distinct refugia, located in the north‐western and south‐eastern coastal lowlands, during Middle Pleistocene interglacial phases, and came into secondary contact following demographic and spatial expansions during the last glacial phase. Main conclusions This scenario of interglacial contraction and glacial expansion is in sharp contrast with patterns commonly observed in temperate species on the continent but parallels recent findings on other Mediterranean island endemics. Such a reverse expansion–contraction (EC) dynamic has been likely associated with glacial increases of climatically suitable coastal lowlands, suggesting this might be a general pattern in Mediterranean island species and also in other coastal regions strongly affected by glacial marine regressions during glacial episodes. This study provides explicit predictions and some methodological recommendations for testing the reverse EC model in other region and taxa

Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation

K.L. was funded by a junior research fellowship from the National Environmental Research Council, UK (NE/I020288/1, NBAF659).Models of speciation-with-gene-flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here, we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced postdivergence gene flow that ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of species divergence which is compatible with theoretical models that posit a role of inversions in speciation with gene flow.Publisher PDFPeer reviewe