Evolutionary Genomics of Adaptation

How DNA sequence divergence leads to phenotypic evolution and adaptation

Overview

Beneath the phenomena of evolutionary adaptation lies a complex lattice in which population-level processes intersect with developmental and genomic constraints. The Cresko Lab explores these multilevel interactions in the threespine stickleback fish, which offers unique advantages as a model system for understanding the genomic basis of adaptation.

The Stickleback Model System

The threespine stickleback provides unparalleled opportunities for studying evolutionary genomics:

Natural Experiments in Evolution

  • Replicate adaptation: Countless independent colonizations of freshwater from marine ancestors
  • Phenotypic radiation: Extensive morphological and physiological diversity within a single species
  • Contemporary evolution: Examples of extremely rapid evolution on human timescales
  • Extant ancestors: Marine populations representing the ancestral state still exist

Experimental Advantages

  • Genetic tractability: Ability to perform controlled crosses in the laboratory
  • Developmental accessibility: External fertilization and transparent embryos
  • Genomic resources: High-quality reference genome and extensive population data
  • CRISPR compatibility: Efficient genome editing for functional validation

Genomic Signatures of Natural Selection

By richly genotyping wild populations and generating controlled laboratory crosses, we investigate:

Population Genomic Patterns

  • Selective sweeps: Identifying regions under strong positive selection
  • Polygenic adaptation: Understanding selection on standing genetic variation
  • Balancing selection: Detecting maintenance of adaptive variation
  • Background selection: Distinguishing selection from demographic processes

Parallel Evolution at the Genomic Level

Our research reveals that a large proportion of the stickleback genome bears signatures of natural selection in replicate adaptations to freshwater: - Identification of parallel genomic regions under selection - Discovery of regulatory vs. coding sequence evolution - Understanding the role of chromosomal inversions in adaptation - Characterizing the genetic architecture of adaptive traits

RAD-seq Innovation and Applications

RAD-seq (Restriction site Associated DNA sequencing), a method pioneered at UO through a Cresko and Johnson lab collaboration, revolutionized population genomics:

Methodological Advances

  • De novo genotyping: Genome-wide marker discovery without reference genomes
  • Cost-effective scaling: Enabling population-level studies in non-model organisms
  • Flexible resolution: Adjustable marker density for different applications
  • Paired-end improvements: Building haplotype blocks for enhanced analyses

Population Genetic Applications

The method enables continuous genomic scans using population genetic statistics: - Detection of outlier loci under selection - Demographic inference and population structure analysis - Phylogeographic reconstruction - Genome-wide association studies (GWAS)

Genomic Architecture of Adaptation

We investigate how genomic organization influences evolutionary processes:

Structural Variation

  • Chromosomal inversions: Their role in maintaining adaptive gene complexes
  • Copy number variation: Gene duplications and deletions in adaptation
  • Transposable elements: Mobile DNA as a source of adaptive variation
  • Recombination landscapes: How recombination rate variation affects adaptation

Gene Regulatory Evolution

  • Cis-regulatory changes: Evolution of gene expression through regulatory mutations
  • Trans-acting factors: Evolution of regulatory networks
  • Epigenetic variation: Heritable changes beyond DNA sequence
  • Gene expression plasticity: Environmental effects on gene regulation

Phylogeography and Population History

Using paired-end RAD-seq data to build haplotype blocks, we employ coalescent approaches to investigate:

Historical Demography

  • Colonization history: Timing and routes of freshwater invasions
  • Population expansions: Demographic changes following colonization
  • Gene flow patterns: Ongoing migration between populations
  • Hybridization zones: Introgression between divergent populations

Molecular Dating

  • Age of adaptive alleles: When beneficial mutations arose or were selected
  • Divergence times: Dating population splits and colonization events
  • Mutation rate calibration: Using known geological events to calibrate molecular clocks
  • Ancestral state reconstruction: Inferring historical character states

Gene-by-Environment Interactions

Understanding how genetic variation interacts with environmental factors:

Environmental Variables

  • Temperature adaptation: Thermal tolerance and performance curves
  • Salinity tolerance: Osmoregulatory adaptations
  • Dietary adaptations: Genetic basis of trophic specialization
  • Parasite resistance: Host-pathogen coevolution

Experimental Approaches

  • Common garden experiments: Separating genetic from environmental effects
  • Reciprocal transplants: Testing local adaptation
  • Selection experiments: Real-time evolution under controlled conditions
  • Plasticity studies: Reaction norm evolution

Current Research Directions

Genomics of Rapid Evolution

  • Tracking allele frequency changes in real-time
  • Understanding the predictability of evolution
  • Identifying constraints on adaptive evolution
  • Measuring the speed of adaptation

Integrative Approaches

  • Connecting genotype to phenotype to fitness
  • Multi-trait analyses of correlated evolution
  • Systems biology of adaptive changes
  • Eco-evolutionary dynamics in nature

Conservation Applications

  • Assessing adaptive potential under climate change
  • Managing genetic diversity in threatened populations
  • Understanding evolutionary responses to human impacts
  • Predicting population resilience

Computational Tools and Resources

We develop and apply cutting-edge computational methods:

Software Development

  • Population genomics pipelines
  • Statistical methods for selection detection
  • Visualization tools for genomic data
  • Machine learning applications

Data Resources

  • Population genomic datasets
  • Annotated variant databases
  • Expression atlases
  • Phenotype-genotype maps

Collaborations

This research involves collaborations with: - Population geneticists worldwide - Computational biologists and bioinformaticians - Evolutionary ecologists - Conservation biologists

Future Directions

Our ongoing and future work aims to: - Integrate long-read sequencing for improved genome assemblies - Develop pangenome resources for stickleback - Apply machine learning to predict adaptive outcomes - Connect molecular evolution to ecosystem function

Learn More

For more information about our evolutionary genomics research: - Contact the Cresko Lab → - View our publications →