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Nosil, P.

Publications and source records attributed to Nosil, P..

7 recordsLinked to original sources

A few genes modulate the ecological impact of a freshwater fish species on food webs and ecosystem functions

Genetic diversity within species can shape food webs and ecosystem functioning as strongly as species diversity, yet the genomic architecture underlying these effects remains unclear. Gene-to-ecosystem relationships may arise from genome-wide diversity, from a limited number of ecologically-important genes, or a combination of both. Experimental tests of these hypotheses are lacking. Here, we manipulated genomic diversity of a top-predatory fish in mesocosms under ambient or warm conditions, and quantified ecological responses spanning fish biomass, prey communities and ecosystem functions. Genome-wide diversity explained few ecological responses, with moderate effects (r=0.260). In contrast, variation at specific candidate SNPs predicted all ecological responses consistently across climatic conditions, with effect sizes being more than twice those of genome-wide estimates (r=0.599). Moreover, combining information from small subsets of candidate SNPs outperformed both single-locus and genome-wide diversity for all ecological responses (r=0.841), consistent with an oligogenic architecture for gene-to-ecosystem relationships. Enrichment analyses revealed functional pathways related to growth, development and metabolic regulation, driven by a small set of pleiotropic genes. We demonstrate that the ecological consequences of intraspecific genetic variation arose from a limited fraction of the genome, highlighting the importance of functional genomic structure, rather than genome-wide diversity alone, in shaping eco-evolutionary dynamics.

ecology↗

Inversion characterization in Timema stick insects: from local PCA to pangenome approaches

Structural variants (SVs) can strongly influence evolutionary processes by suppressing recombination to create jointly inherited regions and by altering gene expression and the 3D organization of DNA. Recent improvements in sequencing technologies have led to an influx of high-resolution genomic data, bolstering research on SVs. When detecting and characterizing SVs, researchers face trade-offs in data and methods concerning scale, resolution, and computational intensity. Here, we evaluate such trade-offs by quantifying how data type, analytical approach, and SV attributes affect the ability to detect and characterize SVs in Timema cristinae stick insects, with a focus on inversions. We specifically evaluate inversions characterized by (i) a population genomic approach based on patterns of local population structure inferred from genotyping-by-sequencing data, (ii) pairwise alignments of eight de novo genome assemblies and SV calling with SyRI, and (iii) a pangenome constructed from the alignment of the eight genome assemblies. Our results suggest that while broad genomic regions harboring SVs can be detected by any of the approaches, the approaches differ in how they characterize inversions, especially small or complex ones. The local population structure approach is exploratory and generally only detects the largest inversions. Pairwise comparative alignments identify the greatest number of inversions, but downstream analyses are influenced by identification of shared inversions across genome pairs. Pangenome approaches are scalable and produce network graphs that describe complex SVs but require a conceptual shift in visualization and interpretation. The collective results highlight limitations and benefits of different approaches in a burgeoning research field.

genomics↗

Dual roles of DNA methylation in gene expression and chromatin structure in a stick insect

Gene body methylation is one of the most taxonomically widespread epigenetic marks, yet its function and evolutionary history are poorly understood. While there is a positive association between gene body methylation and gene expression in many organisms, the mechanisms behind this relationship are unclear. Here, we investigate the function of gene body methylation in the stick insect Timema cristinae. We compare patterns of genome-wide gene body methylation to gene expression, open chromatin peaks, and chromatin compartments. We find that 95% of genes with gene body methylation occur in open chromatin compartments (euchromatin). Furthermore, highly expressed genes are impoverished in methylation at their transcription start site (TSS), which is associated with a peak of open chromatin. These findings suggest that the positive correlation between gene body methylation and gene expression is due to chromatin compartment structure. Yet, methylation around the TSS is associated with gene expression, possibly playing an inhibitory role as in vertebrates. Lastly, comparative analysis of Apis mellifera reveals a similar relationship between methylation and chromatin compartments, but not gene expression. These results suggest a possible explanation for the heterogeneous association between gene body methylation and gene expression and give insight into DNA methylations role in regulating gene expression.

evolutionary biology↗

Genomic regions exhibiting divergent methylation patterns covary with loci associated with mate choice traits in a stick insect

Speciation involves the development of reproductive isolation between diverging populations. A potential key driver of reproductive isolation is mate choice, a behavioural mechanism that can limit gene flow based on divergence in signal traits. While the genetic basis of mating signal traits has been extensively studied, the contribution of epigenetic modifications to their variation remains underexplored, leaving the role of DNA methylation in mate choice unclear. Here, we focus on epigenetic variation and cuticular hydrocarbons (CHCs), the latter being chemical traits used for mate choice in insects. Specifically, we investigate the association between DNA methylation and regions associated with CHC variation in Timema cristinae stick insects. We integrate analyses of differentially methylated regions (DMRs) between individuals from different host-plant ecotypes with genomic sequencing and phenotypic data on CHCs. We find that DMRs are significantly enriched in genetic loci associated with CHCs, suggesting a non-random relationship between DNA methylation and loci associated with these signal traits. While further work is required to clarify causality, our results highlight the potential for epigenetic marks to be associated with traits involved in mate choice. Future studies should thus aim to establish causal links between DNA methylation and signal trait variation, which would clarify the contribution of methylation to mate choice, prezygotic isolation, and ultimately, speciation.

evolutionary biology↗

Ecology not genetics explains correlated trait divergence during speciation

The formation of new species often involves the correlated divergence of multiple traits and genetic regions. However, the mechanisms by which such trait covariation builds up remain poorly understood. In this context, we consider two non-exclusive hypotheses. First, genetic covariance between traits can cause divergent selection on one trait to promote population divergence in correlated traits (a genetic covariation hypothesis). Second, correlated environmental pressures can generate selection on multiple traits, facilitating the evolution of trait complexes (an environmental covariation hypothesis). Here, we test these hypotheses using cryptic coloration (controlled by an incipient supergene) and chemical traits (i.e., cuticular hydrocarbons, CHCs) involved in desiccation resistance and mate choice in Timema cristinae stick insects. We first demonstrate that population divergence in color-pattern is correlated with divergence in some (but not all) CHC traits. We show that when correlated population divergence does occur, it is unlikely to be explained by genetic covariation because within-population genetic covariance between color-pattern and CHCs traits is weak. In contrast, we find that correlated variation in climate and host plant likely generates selection jointly on color-pattern and some CHC traits. This supports the environmental covariation hypothesis, likely via the effects of two correlated environmental axes selecting on different traits. Finally, we provide evidence that misalignment between natural and sexual selection also contributes to patterns of correlated trait divergence. Our results shed light into transitions between phases of speciation by showing that environmental factors can promote population divergence in trait complexes, even without strong genetic covariance.

evolutionary biology↗

The genomics of trait combinations and their influence on adaptive divergence

Understanding rapid adaptation requires quantifying natural selection on traits and elucidating the genotype-phenotype relationship for those traits. However, recent studies have often failed to predict the direction of adaptive allelic variation in natural populations from laboratory studies. Here, we test for genomic signatures of genetic correlations to illustrate how multifarious, correlational selection may drive counterintuitive patterns of population divergence in the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). Apple-infesting populations with relatively early emerging adults have recently evolved from hawthorn-infesting populations consisting of relatively later emerging adults. Multiple studies have reported a paradoxical relationship between population differentiation and seasonal timing, as determined by the timing of diapause termination; alleles associated with late termination occur at higher frequencies in the earlier emerging apple-infesting populations compared to hawthorn-infesting populations. We present evidence that historical selection on diapause termination and another trait, initial diapause intensity, over geographic gradients generated genetic correlations between the traits in a direction antagonistic to contemporary selection on apple-infesting populations. Single nucleotide polymorphism in genomic regions of high linkage disequilibrium associated strongly with diapause termination and intensity, population divergence, geography, and evolutionary responses in laboratory selection experiments. These associations were consistent with geographically variable selection and with correlated evolutionary responses driving higher frequencies of late-associated alleles in the early emerging apple race. In contrast, loci associated only with diapause termination showed the expected pattern (more early-associated alleles in the apple race) in half of the population pairs. Our results suggest that selection on loci demonstrating antagonistic pleiotropy may often shape genomic footprints of rapid adaptation.

evolutionary biology↗

Ecosystem tipping points in an evolving world

There is growing concern over tipping points arising in ecosystems due to the crossing of environmental thresholds. Tipping points lead to strong and possibly irreversible shifts between alternative ecosystem states incurring high societal costs. Traits are central to the feedbacks that maintain alternative ecosystem states, as they govern the responses of populations to environmental change that could stabilize or destabilize ecosystem states. However, we know little about how evolutionary changes in trait distributions over time affect the occurrence of tipping points, and even less about how big scale ecological shifts reciprocally interact with trait dynamics. We argue that interactions between ecological and evolutionary processes should be taken into account for understanding the balance of feedbacks governing tipping points in nature.

ecology↗