Fluctuations in the strength and direction of natural selection through time are a ubiquitous feature of life on Earth. One evolutionary outcome of such fluctuations is adaptive tracking, wherein populations rapidly adapt from standing genetic variation. In certain circumstances, adaptive tracking can lead to the long-term maintenance of functional polymorphism despite allele frequency change due to selection. Although adaptive tracking is likely a common process, we still have a limited understanding of aspects of its genetic architecture and its strength relative to other evolutionary forces such as drift. Drosophila melanogaster living in temperate regions evolve to track seasonal fluctuations and are an excellent system to tackle these gaps in knowledge. By sequencing orchard populations collected across multiple years, we characterized the genomic signal of seasonal demography and identified that the cosmopolitan inversion In(2L)t facilitates seasonal adaptive tracking and shows molecular footprints of selection. A meta-analysis of phenotypic studies shows that seasonal loci within In(2L)t are associated with behavior, life history, physiology, and morphological traits. We identify candidate loci and experimentally link them to phenotype. Our work contributes to our general understanding of fluctuating selection and highlights the evolutionary outcome and dynamics of contemporary selection on inversions.
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 (
- Award ID(s):
- 1753954
- PAR ID:
- 10441428
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
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
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Fraser, Bonnie (Ed.)Abstract Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus that inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time points within a single generation, we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the “number” of moderate changes exceeds the neutral expectation by 10–100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches.more » « less
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