skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Relaxed selection can speed the evolution of complex adaptations
Abstract Natural selection drives adaptive evolution and removes deleterious mutations; these effects are countervailing when a complex adaptation requires mutations that are initially deleterious when they arise, but beneficial in combination. While many models of this dynamic consider how genetic drift or other influences can aid valley crossing by weakening selection, we lack a general, analytical treatment of when relaxed selection might speed this type of adaptation. Here we use simulation and analysis to show that relaxed selection is generally favorable for valley-crossing when adaptive pathways require more than a single deleterious step. We also demonstrate that spatial heterogeneity in selection pressures could, by relaxing selection, allow populations to cross valleys much more rapidly than expected. These results relate to several applications of evolutionary theory to complex systems ranging from host-pathogen evolution to search algorithms in computer science.  more » « less
Award ID(s):
2147101
PAR ID:
10574480
Author(s) / Creator(s):
; ; ;
Publisher / Repository:
bioRxiv
Date Published:
Format(s):
Medium: X
Institution:
bioRxiv
Sponsoring Org:
National Science Foundation
More Like this
  1. Theory predicts that well-adapted populations may evolve mechanisms to counteract the inevitable influx of deleterious mutations. While mutational robustness can be directly selected in the laboratory, evidence for its spontaneous evolution during general adaptation is mixed. Moreover, whether robustness evolves to include pleiotropic effects remains largely unexplored. Here, we studied the effects of point mutations in the RNA polymerase ofEscherichia coliover a 15,000-generation adaptive trajectory. Fitness effects of both beneficial and deleterious mutations were attenuated in fitter backgrounds. In contrast, pleiotropic effects became more severe and widespread with greater adaptation. These results show that trade-offs between robustness and fragility can evolve in regulatory networks, regardless of whether driven by adaptive or nonadaptive processes. More broadly, they illustrate how adaptation can generate hidden variability, with unpredictable evolutionary consequences in new environments. 
    more » « less
  2. Abstract Deleterious variants are selected against but can linger in populations at low frequencies for long periods of time, decreasing fitness and contributing to disease burden in humans and other species. Deleterious variants occur at low frequency but distinguishing deleterious variants from low‐frequency neutral variation is challenging based on population genomics data alone. As a result, we have little sense of the number and identity of deleterious variants in wild populations. For haplodiploid species, it has been hypothesised that deleterious alleles will be directly exposed to selection in haploid males, but selection can be masked in diploid females when deleterious variants are recessive, resulting in more efficient purging of deleterious mutations in males. Therefore, comparisons of the differences between haploid and diploid genomes from the same population may be a useful method for inferring rare deleterious variants. This study provides the first formal test of this hypothesis. Using wild populations of Northern paper wasps (Polistes fuscatus), we find that males have fewer missense and nonsense variants per generation than females from the same population. Allele frequency differences are especially pronounced for rare missense and nonsense variants and these differences lead to a lower mutational load in males than females. Based on these data we infer that many highly deleterious mutations are segregating in the paper wasp population. Stronger selection against deleterious alleles in haploid males may have implications for adaptation in other haplodiploid insects and provides evidence that wild populations harbour abundant deleterious variants. 
    more » « less
  3. Abstract Much theory has focused on how a population’s selfing rate affects the ability of natural selection to remove deleterious mutations from a population. However, most such theory has focused on mutations of a given dominance and fitness effect in isolation. It remains unclear how selfing affects the purging of deleterious mutations in a genome-wide context where mutations with different selection and dominance coefficients co-segregate. Here, we use individual-based forward simulations and analytical models to investigate how mutation, selection and recombination interact with selfing rate to shape genome-wide patterns of mutation accumulation and fitness. In addition to recovering previously described results for how selfing affects the efficacy of selection against mutations of a given dominance class, we find that the interaction of purifying selection against mutations of different dominance classes changes with selfing and recombination rates. In particular, when recombination is low and recessive deleterious mutations are common, outcrossing populations transition from purifying selection to pseudo-overdominance, dramatically reducing the efficacy of selection. At these parameter combinations, the efficacy of selection remains low until populations hit a threshold selfing rate, above which it increases. In contrast, selection is more effective in outcrossing than (partial) selfing populations when recombination rates are moderate to high and recessive deleterious mutations are rare. 
    more » « less
  4. ABSTRACT Invasive species with native ranges spanning strong environmental gradients are well suited for examining the roles of selection and population history in rapid adaptation to new habitats, providing insight into potential evolutionary responses to climate change. The Atlantic oyster drill (Urosalpinx cinerea) is a marine snail whose native range spans the strongest coastal latitudinal temperature gradient in the world, with invasive populations established on the US Pacific coast. Here, we leverage this system using genome‐wide SNPs and environmental data to examine invasion history and identify genotype–environment associations indicative of local adaptation across the native range, and then assess evidence for allelic frequency shifts that would signal rapid adaptation within invasive populations. We demonstrate strong genetic structuring among native regions which aligns with life history expectations, identifying southern New England as the source of invasive populations. Then, we identify putatively thermally adaptive loci across the native range but find no evidence of allele frequency shifts in invasive populations that suggest rapid adaptation to new environments. Our results indicate that while these loci may underpin local thermal adaptation in their native range, selection is relaxed in invasive populations, perhaps due to complex polygenic architecture underlying thermal traits and/or standing capacity for phenotypic plasticity. Given the prolific invasion ofUrosalpinx, our study suggests population success in new environments is influenced by factors other than selection on standing genetic variation that underlies local adaptation in the native range and highlights the importance of considering population history and environmental selection pressures when evaluating adaptive capacity. 
    more » « less
  5. The distribution of fitness effects of mutation plays a central role in constraining protein evolution. The underlying mechanisms by which mutations lead to fitness effects are typically attributed to changes in protein specific activity or abundance. Here, we reveal the importance of a mutation’s collateral fitness effects, which we define as effects that do not derive from changes in the protein’s ability to perform its physiological function. We comprehensively measured the collateral fitness effects of missense mutations in theEscherichia coli TEM-1β-lactamase antibiotic resistance gene using growth competition experiments in the absence of antibiotic. At least 42% of missense mutations inTEM-1were deleterious, indicating that for some proteins collateral fitness effects occur as frequently as effects on protein activity and abundance. Deleterious mutations caused improper posttranslational processing, incorrect disulfide-bond formation, protein aggregation, changes in gene expression, and pleiotropic effects on cell phenotype. Deleterious collateral fitness effects occurred more frequently inTEM-1than deleterious effects on antibiotic resistance in environments with low concentrations of the antibiotic. The surprising prevalence of deleterious collateral fitness effects suggests they may play a role in constraining protein evolution, particularly for highly expressed proteins, for proteins under intermittent selection for their physiological function, and for proteins whose contribution to fitness is buffered against deleterious effects on protein activity and protein abundance. 
    more » « less