Evolution Letters最新文献

A particularly well-studied evolutionary model is the vinegar fly Drosophila melanogaster, a cosmopolitan insect of ancestral southern-central African origin. Recent work suggests that it expanded out of Africa ∼9,000 years ago, and spread from the Middle East into Europe ∼1,800 years ago. During its global expansion, this human commensal adapted to novel climate zones and habitats. Despite much work on phenotypic differentiation and adaptation on several continents (especially North America and Australia), typically in the context of latitudinal clines, little is known about phenotypic divergence among European populations. Here, we sought to provide a continent-wide study of phenotypic differentiation among European populations of D. melanogaster. In a consortium-wide phenomics effort, we assayed 16 fitness-related traits on a panel of 173 isofemale lines from 9 European populations, with the majority of traits measured by several groups using semi-standardized protocols. For most fitness-related traits, we found significant differentiation among populations on a continental scale. Despite inevitable differences in assay conditions among labs, the reproducibility and hence robustness of our measurements were overall remarkably good. Several fitness components (e.g., viability, development time) exhibited significant latitudinal or longitudinal clines, and populations differed markedly in multivariate trait structure. Notably, populations experiencing higher humidity/rainfall and lower maximum temperature showed higher viability, fertility, starvation resistance, and lifespan at the expense of lower heat-shock survival, suggesting a pattern of local adaptation. Our results indicate that derived populations of this tropical fly have been shaped by pervasive spatially varying multivariate selection and adaptation to different climates on the European continent.

When a species colonizes a new environment, it may encounter new parasites to which its immune system is poorly adapted. After an initial spike in infection rates in the naïve founder population, the host may subsequently evolve increased immunity, thereby reducing infection rates. Here, we present an example of this eco-evolutionary process in a population of threespine stickleback (Gasterosteus aculeatus) that was founded in Heisholt Quarry, a man-made quarry pond, in 1967. Marine stickleback rarely encounter Schistocephalus solidus tapeworms (which require freshwater to hatch), and so remain highly susceptible to infection. Initially, introduced marine fish were heavily infected by S. solidus. They exhibited low levels of fibrosis, a heritable immune trait that some genotypes activate in response to infection, thereby suppressing tapeworm growth and viability. By the 1990s, the Heisholt Quarry population exhibited high rates of fibrosis, which partly suppressed S. solidus infection. This increased immune response led to reduced infection rates, and the tapeworm was apparently extirpated by 2021. Because fibrosis has a strong genetic basis in other stickleback populations, we infer that the newly founded stickleback-parasite interaction exhibits an eco-evolutionary process of increased immunity that effectively reduced infection. The infection and immune dynamics documented here closely match those expected from a simple eco-evo dynamic model presented here.

Evolutionary adaptation can allow a population to persist in the face of a new environmental challenge. With many populations now threatened by environmental change, it is important to understand whether this process of evolutionary rescue is feasible under natural conditions, yet work on this topic has been largely theoretical. We used unique long-term data to parameterize deterministic and stochastic models of the contribution of 1 trait to evolutionary rescue using field estimates for the subalpine plant Ipomopsis aggregata and hybrids with its close relative I. tenuituba. In the absence of evolution or plasticity, the 2 studied populations are projected to go locally extinct due to earlier snowmelt under climate change, which imposes drought conditions. Phenotypic selection on specific leaf area (SLA) was estimated in 12 years and multiple populations. Those data on selection and its environmental sensitivity to annual snowmelt timing in the spring were combined with previous data on heritability of the trait, phenotypic plasticity of the trait, and the impact of snowmelt timing on mean absolute fitness. Selection favored low values of SLA (thicker leaves). The evolutionary response to selection on that single trait was insufficient to allow evolutionary rescue by itself, but in combination with phenotypic plasticity it promoted evolutionary rescue in 1 of the 2 populations. The number of years until population size would stop declining and begin to rise again was heavily dependent upon stochastic environmental changes in snowmelt timing around the trend line. Our study illustrates how field estimates of quantitative genetic parameters can be used to predict the likelihood of evolutionary rescue. Although a complete set of parameter estimates are generally unavailable, it may also be possible to predict the general likelihood of evolutionary rescue based on published ranges for phenotypic selection and heritability and the extent to which early snowmelt impacts fitness.

Reversible plasticity, i.e., the ability to deconstruct phenotypic specializations based on environmental conditions, is widespread in nature. Despite its ubiquity, few mathematical models have explored the evolutionary selection pressures that favor trait reversibility. Therefore, many scenarios remain to be examined. In particular, existing theory has modeled trait development as an instantaneous process. These models do not capture the fact that trait development is often a constructive process, in which phenotypes incrementally adjust to local ecologies. Here, we present an optimality model of the evolution of reversible plasticity in which organisms build traits incrementally. In our model, organisms repeatedly sample cues to infer the environmental state-which can vary between generations but not within generations-and incrementally tailor their phenotypes to match their environments. Organisms also have the option to deconstruct phenotypic adjustments. We investigate two different modes of phenotypic deconstruction: Organisms can either deconstruct phenotypic adjustments incrementally or completely deconstruct all phenotypic adjustments in one time period. We highlight two results. First, early-life sensitive periods in construction precede mid-ontogeny sensitive periods in deconstruction. Intriguingly, although organisms typically only deconstruct toward the end of ontogeny, environmental cues in mid-ontogeny have the strongest impact on deconstruction. Second, in contrast to previous models, we find that reversibility often evolves in environments that are stable within generations. Thus, our model shows that reversibility does not require environmental change during development-as long as organisms are initially uncertain about environmental conditions. Our model provides new insights into the capacity for reversibility in species that have evolved in ontogenetically stable environments.

A key prediction of neutral theory is that the level of genetic diversity in a population should scale with population size. However, as was noted by Richard Lewontin in 1974 and reaffirmed by later studies, the slope of the population size-diversity relationship in nature is much weaker than expected under neutral theory. We hypothesize that one contributor to this paradox is that current methods relying on single nucleotide polymorphisms (SNPs) called from aligning short reads to a reference genome underestimate levels of genetic diversity in many species. As a first step to testing this idea, we calculated nucleotide diversity ( $\pi$ ) and $k$ -mer-based metrics of genetic diversity across 112 plant species, amounting to over 205 terabases of DNA sequencing data from 27,488 individuals. After excluding 14 species with low coverage or no variant sites called, we compared how different diversity metrics correlated with proxies of population size that account for both range size and population density variation across species. We found that our population size proxies scaled anywhere from about 3 to over 20 times faster with $k$ -mer diversity than nucleotide diversity after adjusting for evolutionary history, mating system, life cycle habit, cultivation status, and invasiveness. The relationship between $k$ -mer diversity and population size proxies also remains significant after correcting for genome size, whereas the analogous relationship for nucleotide diversity does not. These results are consistent with the possibility that variation not captured by common SNP-based analyses explains part of Lewontin's paradox in plants, but larger scale pangenomic studies are needed to definitively address this question.

The process by which species diverge from one another, gradually accumulate genetic incompatibilities, and eventually reach full-fledged reproductive isolation is a key question in evolutionary biology. However, the nature of reproductive barriers, the pace at which they accumulate, and their genomic distribution remain poorly documented. The disruption of co-adapted epistatic interactions in hybrids and the accumulation of selfish genetic elements are proposed contributors to this process, and can lead to the distortion of the Mendelian segregation of the affected loci across the genome. In this study we detect and quantify segregation distortion across the genomes of crosses produced from a diverse sampling of Arabidopsis lyrata and A. halleri populations, 2 species at the early stages of speciation and that can still interbreed. We observe no distortion loci in crosses with geographically and genetically similar parents, but both their frequency of occurrence and their magnitude become highly variable in more distant crosses. We also observe that distorter loci evolve rapidly, as they occur not only in interspecific hybrids, but also in intraspecific hybrids produced by crossing individuals from 2 isolated regions. Finally, we identify both genome-wide nonindependence and 2 specific genomic regions on different chromosomes where opposite distortion effects are repeatedly observed across multiple F1 individuals, suggesting negative epistasis is a major contributor to the evolution of hybrid segregation distortion. Our study demonstrates that pollen-acting segregation distortion is ubiquitous, and may contribute not only to the ongoing reproductive isolation between A. halleri and A. lyrata, but also between recently diverged populations of the same species.

Cell types are fundamental functional units of multicellular organisms. The evolutionary emergence of new cell types is underpinned by genetic changes, such as gene co-option and cis-regulatory evolution, that propel the assembly or rewiring of molecular networks and give rise to new cell types with specialized functions. Here, we integrate genomic phylostratigraphy with single-cell transcriptomics to explore the evolutionary trends in the assembly of the skeletal cell type-specific gene expression programs. In particular, we investigate how the emergence of lineage-specific genes contributed to this process. We show that osteoblasts and hypertrophic chondrocytes (HC) express evolutionary younger transcriptomes compared to immature chondrocytes that resemble the ancestral skeletogenic program. We demonstrate that the recruitment of lineage-specific genes resulted in subsequent elaboration and individuation of the ancestral chondrogenic gene expression program, propelling the emergence of osteoblasts and HC. Notably, osteoblasts show significant enrichment of vertebrate-specific genes, while HC is enriched in gnathostome-specific genes. By identifying the functional properties of the recruited genes, coupled with the recently discovered fossil evidence, our study challenges the long-standing view on the evolution of vertebrate skeletal structures by suggesting that endochondral ossification and chondrocyte hypertrophy may have already evolved in the last common ancestors of gnathostomes.

Determining the genetic architecture of traits involved in adaptation and speciation is one of the key components of understanding the evolutionary mechanisms behind biological diversification. Hybrid zones provide a unique opportunity to use genetic admixture to identify traits and loci contributing to partial reproductive barriers between taxa. Many studies have focused on the temporal dynamics of hybrid zones, but geographical variation in hybrid zones that span distinct ecological contexts has received less attention. We address this knowledge gap by analyzing hybridization and introgression between black-capped and Carolina chickadees in two geographically remote transects across their extensive hybrid zone, one located in eastern and one in central North America. Previous studies demonstrated that this hybrid zone is moving northward as a result of climate change but is staying consistently narrow due to selection against hybrids. In addition, the hybrid zone is moving ~5× slower in central North America compared to more eastern regions, reflecting continent-wide variation in the rate of climate change. We use whole genome sequencing of 259 individuals to assess whether variation in the rate of hybrid zone movement is reflected in patterns of hybridization and introgression, and which genes and genomic regions show consistently restricted introgression in distinct ecological contexts. Our results highlight substantial similarities between geographically remote transects and reveal large Z-linked chromosomal rearrangements that generate measurable differences in the degree of gene flow between transects. We further use simulations and analyses of climatic data to examine potential factors contributing to continental-scale nuances in selection pressures. We discuss our findings in the context of speciation mechanisms and the importance of sex chromosome inversions in chickadees and other species.

Organisms are already facing climate change. To understand and mitigate the negative effects of climate change on wild and cultivated species, recent research has focused on predicting the fitness of organisms or populations in future climates. The accuracy of these predictions is, however, seldom tested. To test such predictions, we grew a set of 800 genetic families of the annual plant Arabidopsis thaliana in the same field site located in Northern France for 2 consecutive years with contrasted climates. Despite observing, in both years, a clear association between fitness and climatic distance between our field site and the climate of origin of these genetic families, the diverse set of methods we used failed to accurately predict fitness from a year to another. This low accuracy can be explained by the fact that different climatic factors contributed to climate adaptation in different years, which impeded the definition of a meaningful climate descriptor across years. Our results also suggest that populations of A. thaliana from Northern France already suffer from an adaptational lag with respect to climate, and that vegetative growth seems to be a more important trait for climate adaptation than phenology. We discuss the implications of our results for predicting the fitness of wild organisms in future climates and for breeding programs.

[This corrects the article DOI: 10.1093/evlett/qraf002.].