skip to main content


Title: Natural selection drives genome‐wide evolution via chance genetic associations
Abstract

Understanding selection's impact on the genome is a major theme in biology. Functionally neutral genetic regions can be affected indirectly by natural selection, via their statistical association with genes under direct selection. The genomic extent of such indirect selection, particularly across loci not physically linked to those under direct selection, remains poorly understood, as does the time scale at which indirect selection occurs. Here, we use field experiments and genomic data in stick insects, deer mice and stickleback fish to show that widespread statistical associations with genes known to affect fitness cause many genetic loci across the genome to be impacted indirectly by selection. This includes regions physically distant from those directly under selection. Then, focusing on the stick insect system, we show that statistical associations between SNPs and other unknown, causal variants result in additional indirect selection in general and specifically within genomic regions of physically linked loci. This widespread indirect selection necessarily makes aspects of evolution more predictable. Thus, natural selection combines with chance genetic associations to affect genome‐wide evolution across linked and unlinked loci and even in modest‐sized populations. This process has implications for the application of evolutionary principles in basic and applied science.

 
more » « less
Award ID(s):
1844941
NSF-PAR ID:
10366399
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
31
Issue:
2
ISSN:
0962-1083
Page Range / eLocation ID:
p. 467-481
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The study of ecological speciation is inherently linked to the study of selection. Methods for estimating phenotypic selection within a generation based on associations between trait values and fitness (e.g. survival) of individuals are established. These methods attempt to disentangle selection acting directly on a trait from indirect selection caused by correlations with other traits via multivariate statistical approaches (i.e. inference of selection gradients). The estimation of selection on genotypic or genomic variation could also benefit from disentangling direct and indirect selection on genetic loci. However, achieving this goal is difficult with genomic data because the number of potentially correlated genetic loci (p) is very large relative to the number of individuals sampled (n). In other words, the number of model parameters exceeds the number of observations (p ≫ n). We present simulations examining the utility of whole‐genome regression approaches (i.e. Bayesian sparse linear mixed models) for quantifying direct selection in cases wherep ≫ n. Such models have been used for genome‐wide association mapping and are common in artificial breeding. Our results show they hold promise for studies of natural selection in the wild and thus of ecological speciation. But we also demonstrate important limitations to the approach and discuss study designs required for more robust inferences.

     
    more » « less
  2. Abstract

    Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci.

    Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.

     
    more » « less
  3. Abstract

    Understanding how the environment shapes genetic variation provides critical insight about the evolution of local adaptation in natural populations. At multiple spatial scales and multiple geographic contexts within a single species, such information could address a number of fundamental questions about the scale of local adaptation and whether or not the same loci are involved at different spatial scales or geographic contexts. We used landscape genomic approaches from three local elevational transects and rangewide sampling to (a) identify genetic variation underlying local adaptation to environmental gradients in the California endemic oak,Quercus lobata; (b) examine whether putatively adaptive SNPs show signatures of selection at multiple spatial scales; and (c) map putatively adaptive variation to assess the scale and pattern of local adaptation. Of over 10 k single‐nucleotide polymorphisms (SNPs) generated with genotyping‐by‐sequencing, we found signatures of natural selection by climate or local environment at over 600 SNPs (536 loci), some at multiple spatial scales across multiple analyses. Candidate SNPs identified with gene–environment tests (LFMM) at the rangewide scale also showed elevated associations with climate variables compared to the background at both rangewide and elevational transect scales with gradient forest analysis. Some loci overlap with those detected in other oak species, raising the question of whether the same loci might be involved in local climate adaptation in different congeneric species that inhabit different geographic contexts. Mapping landscape patterns of adaptive versus background genetic variation identified regions of marked local adaptation and suggests nonlinear association of candidate SNPs and environmental variables. Taken together, our results offer robust evidence for novel candidate genes for local climate adaptation at multiple spatial scales.

     
    more » « less
  4. Abstract

    Structural variants (SVs) can promote speciation by directly causing reproductive isolation or by suppressing recombination across large genomic regions. Whereas examples of each mechanism have been documented, systematic tests of the role of SVs in speciation are lacking. Here, we take advantage of long‐read (Oxford nanopore) whole‐genome sequencing and a hybrid zone between twoLycaeidesbutterfly taxa (L.melissaand Jackson HoleLycaeides) to comprehensively evaluate genome‐wide patterns of introgression for SVs and relate these patterns to hypotheses about speciation. We found >100,000 SVs segregating within or between the two hybridizing species. SVs and SNPs exhibited similar levels of genetic differentiation between species, with the exception of inversions, which were more differentiated. We detected credible variation in patterns of introgression among SV loci in the hybrid zone, with 562 of 1419 ancestry‐informative SVs exhibiting genomic clines that deviated from null expectations based on genome‐average ancestry. Overall, hybrids exhibited a directional shift towards Jackson HoleLycaeidesancestry at SV loci, consistent with the hypothesis that these loci experienced more selection on average than SNP loci. Surprisingly, we found that deletions, rather than inversions, showed the highest skew towards excess ancestry from Jackson HoleLycaeides. Excess Jackson HoleLycaeidesancestry in hybrids was also especially pronounced for Z‐linked SVs and inversions containing many genes. In conclusion, our results show that SVs are ubiquitous and suggest that SVs in general, but especially deletions, might disproportionately affect hybrid fitness and thus contribute to reproductive isolation.

     
    more » « less
  5. Abstract

    Hybridization facilitates recombination between divergent genetic lineages and can be shaped by both neutral and selective processes. Upon hybridization, loci with no net fitness effects introgress randomly from parental species into the genomes of hybrid individuals. Conversely, alleles from one parental species at some loci may provide a selective advantage to hybrids, resulting in patterns of introgression that do not conform to random expectations. We investigated genomic patterns of differential introgression in natural hybrids of two species of Caribbean anoles,Anolis pulchellusandA. krugiin Puerto Rico. Hybrids exhibitA. pulchellusphenotypes but possessA. krugimitochondrial DNA, originated from multiple, independent hybridization events, and appear to have replaced pureA. pulchellusacross a large area in western Puerto Rico. Combining genome‐wide SNP datasets with bioinformatic methods to identify signals of differential introgression in hybrids, we demonstrate that the genomes of hybrids are dominated bypulchellus‐derived alleles and show only 10%–20%A. krugiancestry. The majority ofA. krugiloci in hybrids exhibit a signal of non‐random differential introgression and include loci linked to genes involved in development and immune function. Three of these genes (delta like canonical notch ligand 1, jagged1 and notch receptor 1) affect cell differentiation and growth and interact with mitochondrial function. Our results suggest that differential non‐random introgression for a subset of loci may be driven by selection favouring the inheritance of compatible mitochondrial and nuclear‐encoded genes in hybrids.

     
    more » « less