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Mugal, C. F.

Publications and source records attributed to Mugal, C. F..

8 recordsLinked to original sources

Regulatory and evolutionary impact of DNA methylation in two songbird species and their naturally occurring F1 hybrids

Regulation of transcription by DNA methylation in 5-CpG-3 context is a widespread mechanism allowing differential expression of genetically identical cells to persist throughout development. Consequently, differences in DNA methylation can reinforce variation in gene expression among cells, tissues, populations and species. Despite a surge in studies on DNA methylation, we know little about the importance of DNA methylation in population differentiation and speciation. Here we investigate the regulatory and evolutionary impact of DNA methylation in five tissues of two Ficedula flycatcher species and their naturally occurring F1 hybrids. We show that the density of CpG in the promoters of genes determines the strength of the association between gene expression and DNA methylation. The impact of DNA methylation on gene expression varies among tissues with brain showing unique patterns. Differentially expressed genes between parental species are predicted by genetic- and methylation differentiation in CpG-rich promoters. However, both these factors fail to predict hybrid misexpression suggesting that promoter mismethylation is not a main determinant of hybrid misexpression in Ficedula flycatchers. Using allele-specific methylation estimates in hybrids we also determine the genome-wide contribution of cis- and trans effects in DNA methylation differentiation. These distinct mechanisms are roughly balanced in all tissues except brain, where trans differences predominate. Overall, this study provides insight on the regulatory and evolutionary impact of DNA methylation in songbirds.

evolutionary biology↗

Evidence that genetic drift not adaptation drives fast-Z and large-Z effects in Ficedula flycatchers

The sex chromosomes have been hypothesized to play a key role in driving adaptation and speciation across many taxa. The reason for this is thought to be the hemizygosity of the heteromorphic part of sex chromosomes in the heterogametic sex, which exposes recessive mutations to natural and sexual selection. The exposure of recessive beneficial mutations increases their rate of fixation on the sex chromosomes, which results in a faster rate of evolution. In addition, genetic incompatibilities between sex-linked loci are exposed faster in the genomic background of hybrids of divergent species, which makes sex chromosomes contribute disproportionately to reproductive isolation. However, in birds, which show a Z/W sex determination system, the disproportionate role of the Z-chromosome in adaptation and reproductive isolation is still debated. Instead, genetic drift has been proposed as the main driver of the so-called fast-Z and large-Z effects in birds. Here, we address this question in Ficedula flycatchers based on population resequencing data of six flycatcher species. Our results provide evidence for both the fast-Z and large-Z effects in Ficedula flycatchers and that these two phenomena are driven by genetic drift rather than positive selection. Genomic scans of selective sweeps and fixed differences in fact suggest a reduced action of positive selection on the Z-chromosome. We propose that the observed reduction in the efficacy of purifying selection on the Z-chromosome helps to establish genetic incompatibilities between Z-linked and autosomal loci, which could result in pronounced selective sweep signatures for compensatory mutations on the autosomes.

evolutionary biology↗

Traditional phylogenetic models are insensitive to variations in the effective population size

A substitution represents the emergence and fixation of an allele in a population or species and is the fundamental event from which phylogenetic models of sequence evolution are devised. Because of the increasing availability of genomic sequences, we are now able to take advantage of intraspecific variability when reconstructing the tree of life. As a result, substitutions can be more realistically modeled as the product of mutation, selection, and genetic drift. However, it is still unclear whether this increased complexity affects our measures of evolutionary times and rates. This study seeks to answer this question by contrasting the traditional substitution model with a population genetic equivalent using data from 4385 individuals distributed across 179 populations and representing 17 species of animals, plants, and fungi. We found that when the population genetics dynamic is modeled via the substitution rates, the evolutionary times and rates of the two models are well correlated, suggesting that the phylogenetic model is able to capture the time and pace of its population counterpart. However, a closer inspection of this result showed that the traditional models largely ignore the effect of the effective population size, even when it is explicitly accounted for in the substitution rates. Our findings suggest that superimposing population-genetics results on the substitution rates is an effective strategy to study mutation and selection biases, while other data sources (e.g., life history traits or polymorphisms) may need to be additionally integrated to make the traditional substitution models sensitive to the impact of genetic drift. When combined with the known effect of ancestral population size on generating phylogenomic incongruence due to incomplete lineage sorting, our findings provide further evidence that unaccounted-for variations in the effective population size may be one of the primary causes of errors in phylogenetic analyses at shorter time scales.

evolutionary biology↗

The genomic basis of hybrid male sterility in Ficedula flycatchers

Identifying genes involved in genetic incompatibilities causing hybrid sterility or inviability is a long-standing challenge in speciation research, especially in studies based on natural hybrid zones. Here we present the first high-probability candidate genes for hybrid male sterility in birds by using a combination of whole genome sequence data, histology sections of testis and single cell transcriptomics of testis samples from male pied-, collared-, and hybrid flycatchers. We reveal failure of meiosis in hybrid males and propose candidate genes involved in genetic incompatibilities causing this failure. Based on identification of genes with non-synonymous fixed differences between the two species and revealing miss-expression patterns of these genes across the various stages of hybrid male spermatogenesis we conclude aberrant chromosome segregation and/or faulty chromatin packing. A lower proportion of spermatids produced by hybrid males implies that a proportion of the aberrant spermatids undergo apoptosis. Finally, we report an overrepresentation of Z-linkage of the revealed candidate incompatibility genes. Our results challenge the assumption that speciation processes are driven by fast evolving genes by showing that a few changes in genes with highly conserved and central functions may quickly ensure reproductive isolation through post-zygotic isolation.

evolutionary biology↗

The role of recombination dynamics in shaping signatures of direct and indirect selection across the Ficedula flycatcher genome

Recombination is a central evolutionary process that reshuffles combinations of alleles along chromosomes, and consequently is expected to influence the efficacy of direct selection via Hill-Robertson interference. Additionally, the indirect effects of selection on neutral genetic diversity are expected to show a negative relationship with recombination rate, as background selection and genetic hitchhiking are stronger when recombination rate is low. However, owing to the limited availability of recombination rate estimates across divergent species, less is known about the impact of evolutionary changes in recombination rate on genomic signatures of selection. To address this question, we estimate recombination rate in two Ficedula flycatcher species, the taiga flycatcher (F. albicilla) and collared flycatcher (F. albicollis). We show that recombination rate is strongly correlated with signatures of indirect selection, and that evolutionary changes in recombination rate between species have observable impacts on this relationship. Conversely, signatures of direct selection on coding sequences show little to no relationship with recombination rate, even when restricted to genes where recombination rate is conserved between species. Thus, using measures of indirect and direct selection that bridge micro- and macro-evolutionary timescales, we demonstrate that the role of recombination rate and its dynamics varies for different signatures of selection.

evolutionary biology↗

Single-Cell Transcriptomics reveals relaxed evolutionary constraint of spermatogenesis in two passerine birds as compared to mammals

Spermatogenesis is a complex process where spermatogonia develop into haploid, mobile sperm cells. The genes guiding this process are subject to an evolutionary trade-off between preserving basic functions of sperm while acquiring new traits ensuring advantages in competition over fertilization of female gametes. In species with XY sex chromosomes, the outcome of this trade-off is found to vary across the stages of spermatogenesis but remains unexplored for species with ZW sex chromosomes. Here we characterize avian spermatogenesis at single cell resolution from testis of collared and pied flycatchers. We find evidence for relaxed evolutionary constraint of genes expressed in spermatocyte cells going through meiosis. An overrepresentation of Z-linked differentially expressed genes between the two species at this stage suggests that this relaxed constraint is associated with the lack of sex-chromosome silencing during meiosis. We conclude that the high throughput of bird spermatogenesis, at least partly, is explained by relaxed developmental constraint.

evolutionary biology↗

The Behavior of Molecular Measures of Natural Selection after a Change in Population Size.

A common model to describe natural selection at the molecular level is the nearly neutral theory, which emphasizes the importance of mutations with slightly deleterious fitness effects as they have a chance to get fixed due to genetic drift. Since genetic drift is stronger in smaller than in larger populations, a negative relationship between molecular measures of selection and population size is expected within the nearly neutral theory. Originally, this hypothesis was formulated under equilibrium conditions. A change in population size, however, pushes the selection-drift balance off equilibrium leading to alterations in the efficacy of selection. To investigate the nonequilibrium behavior, we relate measures of natural selection and genetic drift to each other, considering both, measures of micro- and macroevolution. Specifically, we use a Poisson random field framework to model{pi} N/{pi}S and{omega} as time-dependent measures of selection and assess genetic drift by an effective population size. This analysis reveals a clear deviation from the expected equilibrium selection-drift balance during nonequilibrium periods. Moreover, we find that microevolutionary measures quickly react to a change in population size and reflect a recent change well, at the same time as they quickly lose the knowledge about it. Macroevolutionary measures, on the other hand, react more slowly to a change in population size but instead capture the influence of ancient changes longer. We therefore conclude that it is important to be aware of the different behaviors of micro- and macroevo- lutionary measures when making inference in empirical studies, in particular when comparing results between studies.

evolutionary biology↗

The effects of GC-biased gene conversion on patterns of genetic diversity among and across butterfly genomes

Recombination reshuffles the alleles of a population through crossover and gene conversion. These mechanisms have considerable consequences on the evolution and maintenance of genetic diversity. Crossover, for example, can increase genetic diversity by breaking the linkage between selected and nearby neutral variants. Bias in favor of G or C alleles during gene conversion may instead promote the fixation of one allele over the other, thus decreasing diversity. Mutation bias from G or C to A and T opposes GC-biased gene conversion (gBGC). Less recognized is that these two processes may -when balanced- promote genetic diversity. Here we investigate how gBGC and mutation bias shape genetic diversity patterns in wood white butterflies (Leptidea sp.). This constitutes the first in-depth investigation of gBGC in butterflies. Using 60 re-sequenced genomes from six populations of three species, we find substantial variation in the strength of gBGC across lineages. When modeling the balance of gBGC and mutation bias and comparing analytical results with empirical data, we reject gBGC as the main determinant of genetic diversity in these butterfly species. As alternatives, we consider linked selection and GC content. We find evidence that high values of both reduce diversity. We also show that the joint effects of gBGC and mutation bias can give rise to a diversity pattern which resembles the signature of linked selection. Consequently, gBGC should be considered when interpreting the effects of linked selection on levels of genetic diversity.

evolutionary biology↗