Optimal Allocation Ratios: A Square Root Relationship between the Ratios of Symbiotic Costs and Benefits
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Abstract Coral snakes in the genus Micrurus are venomous, aposematic organisms that signal danger to predators through vivid coloration. Previous studies found that they serve as models to several harmless species of Batesian mimics. However, the extent to which Micrurus species engage in Müllerian mimicry remains poorly understood. We integrate detailed morphological and geographical distribution data to investigate if coral snakes are Müllerian mimics. We found that coloration is spatially structured and that Micrurus species tend to be more similar where they co-occur. Though long supposed, we demonstrate for the first time that coral snakes might indeed be Müllerian mimics as they show some convergence in coloration patterns. Additionally, we found that the length of red-coloured rings in Micrurus is conserved, even at large geographic scales. This finding suggests that bright red rings may be under more substantial stabilizing selection than other aspects of coloration and probably function as a generalized signal for deterring predators.
Abstract Since historical times, the inherent human fascination with pearls turned the freshwater pearl mussel Margaritifera margaritifera (Linnaeus, 1758) into a highly valuable cultural and economic resource. Although pearl harvesting in M. margaritifera is nowadays residual, other human threats have aggravated the species conservation status, especially in Europe. This mussel presents a myriad of rare biological features, e.g. high longevity coupled with low senescence and Doubly Uniparental Inheritance of mitochondrial DNA, for which the underlying molecular mechanisms are poorly known. Here, the first draft genome assembly of M. margaritifera was produced using a combination of Illumina Paired-end and Mate-pair approaches. The genome assembly was 2.4 Gb long, possessing 105,185 scaffolds and a scaffold N50 length of 288,726 bp. The ab initio gene prediction allowed the identification of 35,119 protein-coding genes. This genome represents an essential resource for studying this species’ unique biological and evolutionary features and ultimately will help to develop new tools to promote its conservation.
Abstract Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental variation across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than 15 generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic axes. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified at each scale were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental axis to produce redundant adaptive patterns.
Abstract Giant kelp, Macrocystis pyrifera, exists as distinct morphological variants—or “ecomorphs”—in different populations, yet the mechanism for this variation is uncertain, and environmental drivers for either adaptive or plastic phenotypes have not been identified. The ecomorphs Macrocystis “pyrifera” and M. “integrifolia” are distributed throughout temperate waters of North and South America with almost no geographic overlap and exhibit an incongruous, non-mirrored, distribution across the equator. This study evaluates the degree of genetic divergence between M. “pyrifera” and M. “integrifolia” across 18 populations in Chile and California using whole-genome sequencing and single-nucleotide polymorphism markers. Our results based on a principal component analysis, admixture clustering by genetic similarity, and phylogenetic inference demonstrate that M. “pyrifera” and M. “integrifolia” are genetically distinguishable. Analyses reveal separation by Northern and Southern Hemispheres and between morphs within hemispheres, suggesting that the convergent “integrifolia” morphology arose separately in each hemisphere. This is the first study to use whole-genome sequencing to understand genetic divergence in giant kelp ecomorphs, identifying 83 potential genes under selection and providing novel insights about Macrocystis evolution that were not evident with previous genetic techniques. Future studies are needed to uncover the environmental forces driving local adaptation and presumed convergent evolution of these morphs.
Abstract Polyploidy occurs across the tree of life and is especially common in plants. Because newly formed cytotypes are often incompatible with their progenitors, polyploidy is also said to trigger “instantaneous” speciation. If a polyploid can self-fertilize or reproduce asexually, it is even possible for one individual to produce an entirely new lineage, but how often this scenario occurs is unclear. Here, we investigate the evolutionary history of the wild allotetraploid Mimulus sookensis, which was formed through hybridization between self-compatible, diploid species in the Mimulus guttatus complex. We generate a chromosome-scale reference assembly for M. sookensis and define its distinct subgenomes. Despite previous reports suggesting multiple origins of this highly selfing polyploid, we discover patterns of population genomic variation that provide unambiguous support for a single origin. One M. sookensis subgenome is clearly derived from the selfer Mimulus nasutus, which organellar variation suggests is the maternal progenitor. The ancestor of the other subgenome is less certain, but it shares variation with both Mimulus decorus and M. guttatus, two outcrossing diploids with geographic ranges that overlap broadly with M. sookensis. This study establishes M. sookensis as an example of instantaneous speciation, likely facilitated by the polyploid’s predisposition to self-fertilize.
Abstract The maintenance of genetic variation by balancing selection is of considerable interest to evolutionary biologists. An important but understudied potential driver of balancing selection is antagonistic pleiotropy between diploid and haploid stages of the plant life cycle. Despite sharing a common genome, sporophytes (2n) and gametophytes (n) may undergo differential or even opposing selection. Theoretical work suggests antagonistic pleiotropy between life stages can generate balancing selection and maintain genetic variation. Despite the potential for far-reaching consequences of gametophytic selection, empirical tests of its pleiotropic effects (neutral, synergistic, or antagonistic) on sporophytes are generally lacking. Here, we examined the population genomic signals of selection across life stages in the angiosperm Rumex hastatulus and the moss Ceratodon purpureus. We compared gene expression between life stages and sexes, combined with neutral diversity statistics and the analysis of the distribution of fitness effects. In contrast to what would be predicted under balancing selection due to antagonistic pleiotropy, we found that unbiased genes between life stages were under stronger purifying selection, likely explained by a predominance of synergistic pleiotropy between life stages and strong purifying selection on broadly expressed genes. In addition, we found that 30% of candidate genes under balancing selection in R. hastatulus were located within inversion polymorphisms. Our findings provide novel insights into the genome-wide characteristics and consequences of plant gametophytic selection.
Abstract Analysis of phylogenetic trees has become an essential tool in epidemiology. Likelihood-based methods fit models to phylogenies to draw inferences about the phylodynamics and history of viral transmission. However, these methods are often computationally expensive, which limits the complexity and realism of phylodynamic models and makes them ill-suited for informing policy decisions in real-time during rapidly developing outbreaks. Likelihood-free methods using deep learning are pushing the boundaries of inference beyond these constraints. In this paper, we extend, compare, and contrast a recently developed deep learning method for likelihood-free inference from trees. We trained multiple deep neural networks using phylogenies from simulated outbreaks that spread among 5 locations and found they achieve close to the same levels of accuracy as Bayesian inference under the true simulation model. We compared robustness to model misspecification of a trained neural network to that of a Bayesian method. We found that both models had comparable performance, converging on similar biases. We also implemented a method of uncertainty quantification called conformalized quantile regression that we demonstrate has similar patterns of sensitivity to model misspecification as Bayesian highest posterior density (HPD) and greatly overlap with HPDs, but have lower precision (more conservative). Finally, we trained and tested a neural network against phylogeographic data from a recent study of the SARS-Cov-2 pandemic in Europe and obtained similar estimates of region-specific epidemiological parameters and the location of the common ancestor in Europe. Along with being as accurate and robust as likelihood-based methods, our trained neural networks are on average over 3 orders of magnitude faster after training. Our results support the notion that neural networks can be trained with simulated data to accurately mimic the good and bad statistical properties of the likelihood functions of generative phylogenetic models.
Abstract Accurately reconstructing the reticulate histories of polyploids remains a central challenge for understanding plant evolution. Although phylogenetic networks can provide insights into relationships among polyploid lineages, inferring networks may be hindered by the complexities of homology determination in polyploid taxa. We use simulations to show that phasing alleles from allopolyploid individuals can improve phylogenetic network inference under the multispecies coalescent by obtaining the true network with fewer loci compared with haplotype consensus sequences or sequences with heterozygous bases represented as ambiguity codes. Phased allelic data can also improve divergence time estimates for networks, which is helpful for evaluating allopolyploid speciation hypotheses and proposing mechanisms of speciation. To achieve these outcomes in empirical data, we present a novel pipeline that leverages a recently developed phasing algorithm to reliably phase alleles from polyploids. This pipeline is especially appropriate for target enrichment data, where the depth of coverage is typically high enough to phase entire loci. We provide an empirical example in the North American Dryopteris fern complex that demonstrates insights from phased data as well as the challenges of network inference. We establish that our pipeline (PATÉ: Phased Alleles from Target Enrichment data) is capable of recovering a high proportion of phased loci from both diploids and polyploids. These data may improve network estimates compared with using haplotype consensus assemblies by accurately inferring the direction of gene flow, but statistical nonidentifiability of phylogenetic networks poses a barrier to inferring the evolutionary history of reticulate complexes.
Predicting food web structure in future climates is a pressing goal of ecology. These predictions may be impossible without a solid understanding of the factors that structure current food webs. Here, the most fundamental aspect of food web structure—the relationship between the number of links and species—is still poorly understood. Some species interactions may be physically or physiologically ‘forbidden'—like consumption by non-consumer species—with possible consequences for food web structure. We show that accounting for these ‘forbidden interactions' constrains the feasible link-species space, in tight agreement with empirical data. Rather than following one particular scaling relationship, food webs are distributed throughout this space according to shared biotic and abiotic features. Our study provides new insights into the long-standing question of which factors determine this fundamental aspect of food web structure.
Species displaying temperature-dependent sex determination (TSD) are especially vulnerable to the effects of a rapidly changing global climate due to their profound sensitivity to thermal cues during development. Predicting the consequences of climate change for these species, including skewed offspring sex ratios, depends on understanding how climatic factors interface with features of maternal nesting behaviour to shape the developmental environment. Here, we measure thermal profiles in 86 nests at two geographically distinct sites in the northern and southern regions of the American alligator's ( Alligator mississippiensis ) geographical range, and examine the influence of both climatic factors and maternally driven nest characteristics on nest temperature variation. Changes in daily maximum air temperatures drive annual trends in nest temperatures, while variation in individual nest temperatures is also related to local habitat factors and microclimate characteristics. Without any compensatory nesting behaviours, nest temperatures are projected to increase by 1.6–3.7°C by the year 2100, and these changes are predicted to have dramatic consequences for offspring sex ratios. Exact sex ratio outcomes vary widely depending on site and emission scenario as a function of the unique temperature-by-sex reaction norm exhibited by all crocodilians. By revealing the ecological drivers of nest temperature variation in the American alligator, this study provides important insights into the potential consequences of climate change for crocodilian species, many of which are already threatened by extinction.
ABSTRACT Anthropogenic nitrogen (N) deposition is unequally distributed across space and time, with inputs to terrestrial ecosystems impacted by industry regulations and variations in human activity. Soil carbon (C) content normally controls the fraction of mineralized N that is nitrified ( ƒ nitrified ), affecting N bioavailability for plants and microbes. However, it is unknown whether N deposition has modified the relationships among soil C, net N mineralization, and net nitrification. To test whether N deposition alters the relationship between soil C and net N transformations, we collected soils from coniferous and deciduous forests, grasslands, and residential yards in 14 regions across the contiguous United States that vary in N deposition rates. We quantified rates of net nitrification and N mineralization, soil chemistry (soil C, N, and pH), and microbial biomass and function (as beta‐glucosidase (BG) and N ‐acetylglucosaminidase (NAG) activity) across these regions. Following expectations, soil C was a driver of ƒ nitrified across regions, whereby increasing soil C resulted in a decline in net nitrification and ƒ nitrified . The ƒ nitrified value increased with lower microbial enzymatic investment in N acquisition (increasing BG:NAG ratio) and lower active microbial biomass, providing some evidence that heterotrophic microbial N demand controls the ammonium pool for nitrifiers. However, higher total N deposition increased ƒ nitrified , including for high soil C sites predicted to have low ƒ nitrified , which decreased the role of soil C as a predictor of ƒ nitrified . Notably, the drop in contemporary atmospheric N deposition rates during the 2020 COVID‐19 pandemic did not weaken the effect of N deposition on relationships between soil C and ƒ nitrified . Our results suggest that N deposition can disrupt the relationship between soil C and net N transformations, with this change potentially explained by weaker microbial competition for N. Therefore, past N inputs and soil C should be used together to predict N dynamics across terrestrial ecosystems.
Atmospheric carbon dioxide removal (CDR) is required to stabilize global temperature. CDR can be achieved via ecosystem-based approaches that are cost-effective but reversible (e.g., soil and forest management) or by more durable but expensive approaches (e.g., direct air capture coupled with geologic storage). Here, we examine trade-offs between these approaches, focusing on timing, climate impacts, and cost. We simulated reversible carbon accrual for a range of CDR contract structures using a general minimalist model of ecosystem carbon cycling, and parameterized it to simulate US agricultural soil management─specifically cover cropping─as a case study. We then quantified the resulting impact on atmospheric carbon and global temperature using a climate model emulator. We find that maintaining a patchwork of reversible CDR projects by replacing lapsed projects with new projects can reduce warming by 22–195 μ°C in 2100 and that the magnitude of this cooling effect depends on how effectively the patchwork is maintained. Long-term maintenance of reversible CDR projects requires institutional stability that cannot be guaranteed over multiple decades. Consequently, effective CDR ultimately requires replacing reversible projects with durable projects. To address this problem, we modeled the cost of replacing reversible agricultural soil CDR with geologic CDR. We found that using reversible CDR as a bridge to durable CDR is potentially more cost-effective as a global cooling strategy (0.20–0.81 billion USD per μ°C avoided) than perpetual maintenance of reversible CDR (0.32–1.31 billion USD per μ°C avoided) or an immediate transition to durable CDR (1.37–2.19 billion USD per μ°C avoided). However, we emphasize that institutional commitments to maintain reversible CDR projects cannot be guaranteed. Reliance on reversible CDR as a bridge to durable CDR therefore carries an unknown amount of risk and will only function if efforts to maintain reversible CDR are robust.
R code associated with "Assessing the Effect of a Deep-Rooted Grass on Belowground Carbon Storage in Cultivated Land: Insights from a Multi-Site US Study" These scripts can be used to analyze the accompanying dataset: https://doi.org/10.5281/zenodo.16620529. (1) resampling_functions.R : Creates functions for resampling data for nonparametric bootstrapping (2) bootstrap_depth_profiles.R : Applies resampling functions to the dataset (3) gapfill_masscalcs.R : Prepares data for equivalent mass calculations (4) get_14C_EM.R : Applies soilR to obtain the 14C end member for mixing model calculations (5) mass_aggregate.R : Performs equivalent mass and mass weighted averaging calculations.
Bacterial species often undergo rampant recombination yet maintain cohesive genomic identity. Ecological differences can generate recombination barriers between species and sustain genomic clusters in the short term. But can these forces prevent genomic mixing during long-term coevolution? Cyanobacteria in Yellowstone hot springs comprise several diverse species that have coevolved for hundreds of thousands of years, providing a rare natural experiment. By analyzing more than 300 single-cell genomes, we show that despite each species forming a distinct genomic cluster, much of the diversity within species is the result of hybridization driven by selection, which has mixed their ancestral genotypes. This widespread mixing is contrary to the prevailing view that ecological barriers can maintain cohesive bacterial species and highlights the importance of hybridization as a source of genomic diversity.
All relative analysis data and codes used in this study are available on the Figshare data repository. You can also find the codes on the Github repository at https://github.com/vnuii/Y1000_gene_family.
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Human activity impacts the evolutionary trajectories of many species worldwide. Global trade of agricultural goods contributes to the dispersal of pathogens reshaping their genetic makeup and providing opportunities for virulence gains. Understanding how pathogens surmount control strategies and cope with new climates is crucial to predicting the future impact of crop pathogens. Here, we address this by assembling a global thousand-genome panel of Zymoseptoria tritici, a major fungal pathogen of wheat reported in all production areas worldwide. We identify the global invasion routes and ongoing genetic exchange of the pathogen among wheat-growing regions. We find that the global expansion was accompanied by increased activity of transposable elements and weakened genomic defenses. Finally, we find significant standing variation for adaptation to new climates encountered during the global spread. Our work shows how large population genomic panels enable deep insights into the evolutionary trajectory of a major crop pathogen.