Ehrlich, M. A. | bioRxiv Science

bioRxiv2023

Relentless Selection: The importance of within-generation selection in heterogeneous habitats

Natural selection relentlessly reshapes the genetic and phenotypic composition of populations, yet often adaptations cannot emerge due to excessive migration and gene flow. Nevertheless, in heterogeneous habitats strong selection could temporarily establish significant trait divergence among environmental patches. Here, we show that in Fundulus heteroclitus, a single generation of selection drives significant phenotypic divergence (5-15%) in organismal metabolic rate, cardiac metabolic rate and hypoxia tolerance. This divergence occurs among individuals of the same panmictic population residing in environmentally distinct microhabitats. Phenotypic divergence remains observable following long-term common-gardening and is supported by previous work documenting fine-scale, genetic divergence among microhabitat residents. We show that the magnitude of within-generation trait divergence is on the order of what is commonly observed among more isolated populations that have diverged over multiple generations. Although panmictic reproduction among microhabitat residents erodes trait divergence every generation, strong selection could potentially reestablish it in the next. In heterogeneous habitats, transient, fine-scale divergence could have a considerable impact on eco-evolutionary dynamics. Ignoring its contribution to overall trait variance could limit our ability to define meaningful, evolved divergence. SummaryNatural selection can lead to changes in organisms traits over time. Typically, these changes occur slowly over multiple generations and over large spatial scales. By studying a wild population of Atlantic killifish, we show that a single generation of natural selection can generate substantial trait variation over short distances. We observe significant differences in several physiological traits among individuals inhabiting distinct microhabitats in a patchy salt marsh environment. These differences are unlikely due to physiological acclimation and are best explained by strong, natural selection removing those individuals not suited to a particular microhabitat. Previous studies support natural selection as the most likely explanation, having shown subtle genetic differences among microhabitat residents. Remarkably, the magnitude of trait divergence is on the order of what is typically observed among populations that have diverged over multiple generations and larger spatial scales. Our results highlight the significant contribution of natural selection to trait variation in patchy environments, even over exceptionally short time and small spatial scales.

evolutionary biology↗

bioRxiv2020

Rapid polygenic selection generates fine spatial structure among ecological niches in a well-mixed population

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. Author SummaryEvolution by adaptation to local environmental conditions may occur more rapidly than previously thought. Recent studies show that natural selection is extremely effective when acting on, not one, but multiple genetic variants that are already present in a population. Here, we show that polygenic selection can lead to adaptation within a single generation by studying a wild, well-mixed population of mud minnows inhabiting environmentally distinct locations or niches (i.e. tidal ponds and coastal basins). We monitor allele proportions at over 10,000 genetic variants over time within a single generation and find a significant number to be changing substantially in every niche, suggestive of natural selection. We further demonstrate this genetic change to be non-random, generating mild, yet significant divergence between residents inhabiting distinct niches, indicative of local adaptation. We corroborate a previous study which discovered similar genetic divergence among niches during a different year, suggesting that local adaptation via natural selection occurs every generation. We show polygenic selection on standing genetic variation to be an effective and evolutionarily inexpensive mechanism, allowing organisms to rapidly adapt to their environments even at extremely short time scales. Our study provides valuable insights into the rate of evolution and the ability of organisms to respond to environmental change.

evolutionary biology↗