The evolutionary stability of quantitative traits depends on whether a population can resist invasion by any mutant. While uninvadability is well understood in well-mixed populations, it is much less so in subdivided populations when multiple traits evolve jointly. Here, we investigate whether a spatially subdivided population at a monomorphic equilibrium for multiple traits can withstand invasion by any mutant, or is subject to diversifying selection. Our model also explores the among traits correlations arising from diversifying selection and how they depend on relatedness due to limited dispersal. We find that selection favours a positive (negative) correlation between two traits, when the selective effects of one trait on relatedness is positively (negatively) correlated to the indirect fitness effects of the other trait. We study the evolution of traits for which this matters: dispersal that decreases relatedness, and helping that has positive indirect fitness effects. We find that when dispersal cost is low and the benefits of helping accelerate faster than its costs, selection leads to the coexistence of mobile defectors and sessile helpers. Otherwise, the population evolves to a monomorphic state with intermediate helping and dispersal. Overall, our results highlight the importance of population subdivision for evolutionary stability and correlations among traits.

Urbanization significantly alters natural ecosystems, and its rate is only expected to increase globally as more humans move into urban centers. Urbanized landscapes are often highly fragmented. Isolated populations within these fragments may adapt in response to novel urban ecosystems, but few studies have found strong evidence of evolutionary responses in urban environments. We used multiple genome scan and genotype-environment association (GEA) approaches to examine signatures of selection in transcriptomes from urban white-footed mice (Peromyscus leucopus) in New York City. We scanned transcriptomes from 48 P. leucopus individuals from six environmentally heterogeneous locations (three urban and three rural) for evidence of rapid local adaption in isolated urban habitats. We analyzed 154,770 SNPs and identified patterns of genetic differentiation between urban and rural sites and signatures of selection in a large subset of genes. Neutral demographic processes can create allele frequency patterns that are indistinguishable from positive selection. We accounted for this by simulating a neutral SNP dataset under the inferred demographic history for the sampled P. leucopus populations to serve as a null model when choosing outliers. We annotated the resulting outlier genes and further validated them by associating allele frequency differences with environmental measures of urbanization, percent impervious surface and human population density. The majority of candidate genes were involved in metabolic functions, especially dietary specialization. A subset of these genes have well-established roles in metabolizing lipids and carbohydrates, including transport of cholesterol and desaturation of fatty acids. Our results reveal clear genetic differentiation between rural and urban sites that likely resulted from rapid local adaptation in urbanizing habitats. The specific candidate loci that we identified suggest that populations of P. leucopus are using novel food resources in urban habitats or locally adapting through changes in their metabolism. Our data support the idea that cities represent novel ecosystems with a unique set of selective pressures.

The Allee effect is a theoretical model predicting low growth rates and the possible extinction of small populations. Historically, studies of the Allee effect have focused on demography. As a result, underlying processes other than the direct effect of population density on fitness components are not generally taken into account. There has been heated debate about the potential of genetic processes to drive small populations to extinction, but such processes clearly do have an impact on small populations over short time scales, and some may generate Allee effects. However, as opposed to the ecological Allee effect, which is underpinned by cooperative interactions between individuals, genetically driven Allee effects require a change in genetic structure to link the decline in population size with a decrease in fitness components. We therefore define the genetic Allee effect as a two-step process whereby a decrease in population size leads to a change in population genetic structure, and in turn, to a decrease in individual fitness. We describe potential underlying mechanisms, and review the evidence for this original type of component Allee effect, using published examples from both plants and animals. The possibility of considering demogenetic feedback in light of genetic Allee effects clarifies the analysis and interpretation of demographic and genetic processes, and the interplay between them, in small populations.

Biological aging is characterized by an age-dependent increase in the probability of death and by a decrease in the reproductive capacity. Individual age-dependent rates of survival and reproduction have a strong impact on population dynamics, and the genetic elements determining survival and reproduction are under different selective forces throughout an organism lifespan. Here we develop a highly versatile numerical model of genome evolution – both asexual and sexual – for a population of virtual individuals with overlapping generations, where the genetic elements affecting survival and reproduction rate at different life stages are free to evolve due to mutation and selection. Our model recapitulates several emerging properties of natural populations, developing longer reproductive lifespan under stable conditions and shorter survival and reproduction in unstable environments. Faster aging results as the consequence of the reduced strength of purifying selection in more unstable populations, which have large portions of the genome that accumulate detrimental mutations. Unlike sexually reproducing populations under constant resources, asexually reproducing populations fail to develop an age-dependent increase in death rates and decrease in reproduction rates, therefore escaping senescence. Our model provides a powerful in silico framework to simulate how populations and genomes change in the context of biological aging and opens a novel analytical opportunity to characterize how real populations evolve their specific aging dynamics.

Since their endosymbiotic origin, mitochondria have lost most of their genes. Despite the central cellular importance of mtDNA, selective mechanisms underlying the evolution of its content across eukaryotes remain contentious, with no data-driven exploration of different hypotheses. We developed HyperTraPS, a powerful methodology coupling stochastic modelling with Bayesian inference to identify the ordering and causes of evolutionary events. Using a large dataset from over 2000 complete mitochondrial genomes, we inferred evolutionary trajectories of mtDNA gene loss across the eukaryotic tree of life. We find that proteins fulfilling central energetic roles in the assembly of mitochondrial complexes are prefentially retained in mitochondria across eukaryotes, biophysically supporting `colocalization for redox regulation’. We also provide the first quantitative evidence that a combination of GC content and protein hydrophobicity is required to explain mtDNA gene retention, and predicts the success of artificial gene transfer experiments. Our results demonstrate that a combination of these three characteristics explains most mtDNA gene variability, addressing the long-debated question of why particular genes are retained in mitochondrial genomes.

We use genome-wide data from the third generation respondents of the Framingham Heart Study to estimate heritability in body mass index using different quantities of the measured genotype. Heritability decreases rapidly when SNPs implicated by a genome-wide association study are removed but shows essentially no decline when SNPs implicated by a gene-environment interaction in a second genome-wide analysis are removed. This second result is highlighted by our additional finding that the SNPs which explain heritability amongst a subsample defined by higher educational attainment explain no heritability of the heritability in the lower education group, and vice-versa. Finally, we do find consistent heritability estimates when we compare family-based estimates versus those based on measured genotype.