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: Adaptation to distinct habitats is maintained by contrasting selection at different life stages in sunflower ecotypes
Abstract Conspecific populations living in adjacent but contrasting microenvironments represent excellent systems for studying natural selection. These systems are valuable because gene flow is expected to force genetic homogeneity except at loci experiencing divergent selection. A history of reciprocal transplant and common garden studies in such systems, and a growing number of genomic studies, have contributed to understanding how selection operates in natural populations. While selection can vary across different fitness components and life stages, few studies have investigated how this ultimately affects allele frequencies and the maintenance of divergence between populations. Here, we study two sunflower ecotypes in distinct, adjacent habitats by combining demographic models with genome‐wide sequence data to estimate fitness and allele frequency change at multiple life stages. This framework allows us to estimate that only local ecotypes are likely to experience positive population growth (λ > 1) and that the maintenance of divergent adaptation appears to be mediated via habitat‐ and life stage‐specific selection. We identify genetic variation, significantly driven by loci in chromosomal inversions, associated with different life history strategies in neighbouring ecotypes that optimize different fitness components and may contribute to the maintenance of distinct ecotypes.  more » « less
Award ID(s):
1753954
PAR ID:
10441428
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ABSTRACT Tree species are often locally adapted to their environments, but the extent to which environmental adaptation contributes to incipient speciation is unclear. One of the rarest pines in the world, Torrey pine (Pinus torreyanaParry), persists naturally across one island and one mainland population in southern California. The two populations are morphologically and genetically differentiated but experience some connectivity, making it an ideal system for assessing the evolution of reproductive isolation. Previous work has found evidence of heterosis in F1 mainland‐island hybrids, suggesting genetic rescue could be beneficial in the absence of reproductive barriers. Using ddRADseq and GWAS for a common garden experiment of island, mainland, and F1 individuals, we identified candidate loci for environmentally driven reproductive isolation, their function, and their relationship to fitness proxies. By simulating neutral evolution and admixture between the two populations, we identified loci that exhibited reduced heterozygosity in the F1s, evidence of selection against admixture. SNPs with reduced F1 heterozygosity were enriched for growth and pollination functions, suggesting genetic variants that could be involved in the evolution of reproductive barriers between populations. One locus with reduced F1 heterozygosity exhibited strong associations with growth and reproductive fitness proxies in the common garden, with the mainland allele conferring increased fitness. If this locus experiences divergent selection in the two natural populations, it could promote their reproductive isolation. Finally, although hybridization largely reduced allele fixation in the F1s initially, indicating heterosis is likely due to the masking of deleterious alleles, the emergence of reproductive isolation between populations may diminish the longer‐term benefits of genetic rescue in F2 or advanced‐generation hybrids. As Torrey pine is a candidate for interpopulation genetic rescue, caution is warranted where longer‐term gene flow between diverged populations may result in reduced fitness if barriers have evolved. 
    more » « less
  2. Synopsis The presence of standing genetic variation will play a role in determining a population's capacity to adapt to environmentally relevant stressors. In the Gulf of Mexico, extreme climatic events and anthropogenic changes to local hydrology will expose productive oyster breeding grounds to stressful low salinity conditions. We identified genetic variation for performance under low salinity (due to the combined effects of low salinity and genetic load) using a single-generation selection experiment on larvae from two populations of the eastern oyster, Crassostrea virginica. We used pool-sequencing to test for allele frequency differences at 152 salinity-associated genes for larval families pre- and post-low salinity exposure. Our results have implications for how evolutionary change occurs during early life history stages at environmentally relevant salinities. Consistent with observations of high genetic load observed in oysters, we demonstrate evidence for purging of deleterious alleles at the larval stage in C. virginica. In addition, we observe increases in allele frequencies at multiple loci, suggesting that natural selection for low salinity performance at the larval stage can act as a filter for genotypes found in adult populations. 
    more » « less
  3. Evolution by natural selection may be effective enough to allow for recurrent, rapid adaptation to distinct niche environments within a well-mixed population. For this to occur, selection must act on standing genetic variation such that mortality i.e. genetic load, is minimized while polymorphism is maintained. Selection on multiple, redundant loci of small effect provides a potentially inexpensive solution. Yet, demonstrating adaptation via redundant, polygenic selection in the wild remains extremely challenging because low per-locus effect sizes and high genetic redundancy severely reduce statistical power. One approach to facilitate identification of loci underlying polygenic selection is to harness natural replicate populations experiencing similar selection pressures that harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus. F. heteroclitus inhabits salt marsh estuaries that are characterized by high environmental heterogeneity e.g. tidal ponds, creeks, coastal basins. Here, we sample four of these heterogeneous niches (one coastal basin and three replicate tidal ponds) at two time points from among a single, panmictic F. heteroclitus population. We identify 10,861 single nucleotide polymorphisms using a genotyping-by-sequencing approach and quantify temporal allele frequency change within, as well as spatial divergence among subpopulations residing in these niches. We find a significantly elevated number of concordant allele frequency changes among all subpopulations, suggesting ecosystem-wide adaptation to a common selection pressure. Remarkably, we also find an unexpected number of temporal allele frequency changes that generate fine-scale divergence among subpopulations, suggestive of local adaptation to distinct niche environments. Both patterns are characterized by a lack of large-effect loci yet an elevated total number of significant loci. Adaptation via redundant, polygenic selection offers a likely explanation for these patterns as well as a potential mechanism for polymorphism maintenance in the F. heteroclitus system. 
    more » « less
  4. null (Ed.)
    Interactions among selection, gene flow, and drift affect the trajectory of adaptive evolution. In natural populations, the direction and magnitude of these processes can be variable across different spatial, temporal, or ontogenetic scales. Consequently, variability in evolutionary processes affects the predictability or stochasticity of microevolutionary outcomes. We studied an intertidal fish, Bathygobius cocosensis (Bleeker, 1854), to understand how space, time, and life stage structure genetic and phenotypic variation in a species with potentially extensive dispersal and a complex life cycle (larval dispersal preceding benthic recruitment). We sampled juvenile and adult life stages, at three sites, over three years. Genome-wide SNPs uncovered a pattern of chaotic genetic patchiness, that is, weak-but-significant patchy spatial genetic structure that was variable through time and between life stages. Outlier locus analyses suggested that targets of spatially divergent selection were mostly temporally variable, though a significant number of spatial outlier loci were shared between life stages. Head shape, a putatively ecologically responsive (adaptive) phenotype in B. cocosensis also exhibited high temporal variability within sites. However, consistent spatial relationships between sites indicated that environmental similarities among sites may generate predictable phenotype distributions across space. Our study highlights the complex microevolutionary dynamics of marine systems, where consideration of multiple ecological dimensions can reveal both predictable and stochastic patterns in the distributions of genetic and phenotypic variation. Such considerations probably apply to species that possess short, complex life cycles, have large dispersal potential and fecundities, and that inhabit heterogeneous environments. 
    more » « less
  5. Complex life cycles, in which discrete life stages of the same organism differ in form or function and often occupy different ecological niches, are common in nature. Because stages share the same genome, selective effects on one stage may have cascading consequences through the entire life cycle. Theoretical and empirical studies have not yet generated clear predictions about how life cycle complexity will influence patterns of adaptation in response to rapidly changing environments or tested theoretical predictions for fitness trade-offs (or lack thereof) across life stages. We discuss complex life cycle evolution and outline three hypotheses—ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy—for how selection may operate on organisms with complex life cycles. We suggest a within-generation experimental design that promises significant insight into composite selection across life cycle stages. As part of this design, we conducted simulations to determine the power needed to detect selection across a life cycle using a population genetic framework. This analysis demonstrated that recently published studies reporting within-generation selection were underpowered to detect small allele frequency changes (approx. 0.1). The power analysis indicates challenging but attainable sampling requirements for many systems, though plants and marine invertebrates with high fecundity are excellent systems for exploring how organisms with complex life cycles may adapt to climate change. 
    more » « less