The effects of migration on evolutionary dynamics in natural populations of Drosophila melanogaster

Ozan Kiratli

2022-07-15

Evolution 101 & Introduction

Evolution 101

  • Evolutionary Forces
    • Selection, Drift, Mutations, Gene Flow
  • Basis for Adaptation
  • Rapid Adaptation
  • Epistasis

Evolutionary forces

Evolutionary forces: Drift

Evolutionary forces: Selection

Evolutionary forces: Selection - Local adaptation

Evolutionary forces: Mutations

Evolutionary forces: Gene flow

Adaptive Consequences of Gene Flow

Assumptions of the current theory

  • Evolution is slow and it cannot keep up with ecological changes.
  • Evolutionary and ecological timescales are separate.

Rapidly and dynamically changing environments

Revisiting Gene flow - Changing environments

Rapid adaptation

Basis of Adaptive Response

  • Phenotypic variation
  • Differential fitness
  • Heritability of these traits

Basis of Adaptive Response

  • Phenotypic variation
  • Differential fitness
  • Heritability of these traits

Basis of Adaptive Response

  • Phenotypic variation
  • Differential fitness
  • Heritability of these traits

Basis of Adaptive Response

  • Phenotypic variation
  • Differential fitness
  • Heritability of these traits

Basis of Adaptive Response

  • Phenotypic variation
  • Differential fitness
  • Heritability of these traits

Genetic Architecture of Fitness-Associated Traits

Epistasis

  • Functional
  • Statistical

Epistasis - Functional

  • Functional
  • Statistical

Epistasis - Statistical

  • Functional
  • Statistical

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Genetic architecture of complex traits

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Dynamically changing environments
  • Rapid adaptive responses
  • Pervasive epistasis in complex traits

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Dynamically changing environments
  • Rapid adaptive responses
  • Pervasive epistasis in complex traits

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Dynamically changing environments
  • Rapid adaptive responses
  • Pervasive epistasis in complex traits

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Dynamically changing environments
  • Rapid adaptive responses
  • Pervasive epistasis in complex traits
  • Epistasis can be adaptive

Gene Flow - Epistasis - Rapid Adaptation

  • Classical understanding
  • Dynamically changing environments
  • Rapid adaptive responses
  • Pervasive epistasis in complex traits
  • Epistasis can be adaptive
  • Gene flow can also be adaptive

Migration Events

Let’s consider a simple model

Migration Events

Let’s consider a simple model

  • Focal population \(F\)

\(F\)

Migration Events

Let’s consider a simple model

  • Focal population \(F\)
  • Migrant population \(M\)

\(F\)

\(M\)

Migration Events

Let’s consider a simple model

  • Focal population \(F\)
  • Migrant population \(M\)
  • Unidirectional Migration
    • From \(M\) to \(F\)
    • Single time

\(F\)

\(M\)

Fitness Effects of a Single Migration Event: Predictions

  1. No effect on fitness
  • \(F\) and \(M\) are locally adapted, high levels of isolation, migration results in no gene flow
  • \(F\) and \(M\) have similar trait values in focal environment, gene interactions are additive

Fitness Effects of a Single Migration Event: Predictions

  1. No effect on fitness
  1. Decreases fitness
  • \(F\) and \(M\) are locally adapted, gene interactions are additive
  • \(F\) and \(M\) have similar trait values in focal environment, gene interactions are dominated by negative epistasis

Fitness Effects of a Single Migration Event: Predictions

  1. No effect on fitness
  1. Decreases fitness
  1. Increases fitness
  • Regardless of being locally adapted, gene interactions are dominated by positive epistasis

Adaptive Consequences of a Single Migration Event: Predictions

  1. No effect

Adaptive Consequences of a Single Migration Event: Predictions

  1. No effect
  1. Impedes adaptation
  • Dobzhansky Muller Incompatibilities
  • Swamping etc.
  • Decreased fitness after migration with possible recovery to under original fitness

Adaptive Consequences of a Single Migration Event: Predictions

  1. No effect
  1. Impedes adaptation
  1. Facilitates adaptation
  • Variation is good regardless of the source (assumes positive epistasis)
    • Always increased fitness
  • Condition dependent (can be a mix of positive and negative epistasis)
    • Decreased fitness followed by increasing fitness after several generations

Best(!) Model System: Drosophila melanogaster

Population Demography of D. melanogaster

Singh and Long (1992)

Local Adaptation and Latitudinal Clines

Adrion et al. (2015)

Rapid Adaptation

Rudman et al. (2022)

Direct Experiments on the Effects of Migration on Rapid Adaption

Research Questions

  • Does migration result in enough gene flow to affect populations?
  • What is the effect of migration on rapid adaptation?
    • No effect, facilitate, or impede
  • What is the relationship between variation and the adaptive response?
    • Amount of variation vs. the nature of variation

Research Hypothesis

  • Single time large migration event from a remote population to a focal population, after temperature mediated selection, might:
    • Have no effects on the adaptive response
    • Impede adaptation by decreasing the response
    • Facilitate adaptation by increasing the response

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Experimental Design

Results

Results: Fitness Effects of 1:1 Gene Flow

Results: Gene Flow as a Result of a Migration Event

F PF P PM
PF 137.115
P 148.423 77.341
PM 144.548 68.203 75.732
M 157.985 97.717 100.952 89.629

Results: Rapid Adaptation

Trait Selection greater less
Development Time Summer-like 1.00000 0.03125*
Development Time Fall-like 0.03125* 1.00000
Viability Summer-like 0.03125* 1.00000
Viability Fall-like 0.03125 1.00000
Fecundity Summer-like 1.00000 0.03125*
Fecundity Fall-like 0.96875 0.06250
Heat Tolerance (Females) Summer-like 1.00000 0.03125*
Heat Tolerance (Females) Fall-like 1.00000 0.03125*
Heat Tolerance (Males) Summer-like 1.00000 0.03125*
Heat Tolerance (Males) Fall-like 1.00000 0.03125*
Starvation Resistance (Females) Summer-like 0.78125 0.31250*
Starvation Resistance (Females) Fall-like 1.00000 0.03125*
Starvation Resistance (Males) Summer-like 0.90625 0.15625
Starvation Resistance (Males) Fall-like 0.93750 0.09375
Trait greater less
Development Time 0.03125* 1.00000
Viability 0.78125 0.31250
Fecundity 0.03125* 1.00000
Heat Tolerance (Females) 0.93750 0.09375
Heat Tolerance (Males) 0.03125* 1.00000
Starvation Resistance (Females) 1.00000 0.03125*
Starvation Resistance (Males) 0.40625 0.68750

Results: Rapid Adaptation

Results: Temperature-mediated adaptation

Df Pillai approx F num Df den Df Pr(>F)
Selection 1 0.853 111.454 6 115 1.52e-45 ***
Time 1 0.782 68.814 6 115 9.45e-36 ***
Population 4 0.831 5.160 24 472 2.08e-13 ***
Selection:Time 1 0.853 111.454 6 115 1.52e-45 ***
Selection:Population 4 0.175 0.901 24 472 6.01e-01
Time:Population 4 0.430 2.367 24 472 3.26e-04 ***
Selection:Time:Population 4 0.175 0.901 24 472 6.01e-01
Residuals 120 NA NA NA NA NA

Results: Gene Flow Facilitated Adaptive Response

Time Selection Population greater less
Pre-selection PF vs PF[sim] 0.69514 0.304863
Pre-selection PM vs PM[sim] 0.99832 0.001681**
Post-selection Summer-like PF vs PF[sim] 0.98807 0.011932*
Post-selection Summer-like PM vs PM[sim] 0.99933 0.000671***
Post-selection Fall-like PF vs PF[sim] 0.02150* 0.978500
Post-selection Fall-like PM vs PM[sim] 0.00416** 0.995844

Results: Lab - Field Palallelism

Results: Epistasis

  1. No effect
  1. Impedes adaptation
  1. Facilitates adaptation
  • Variation is good regardless of the source (assumes positive epistasis)
    • Always increased fitness
  • Condition dependent (can be a mix of positive and negative epistasis)
    • Decreased fitness followed by increasing fitness after several generations

Summary

  • Migration events resulted in gene flow
  • Observations of rapid adaptation
    • Direct response to selection in only 5 generations
    • Differential response to selection regimes
  • Parallel responses to both selection regimes across populations
  • Temperature as the main driver of these responses
  • Adaptive role of migration
  • Epistatic interactions driving adaptation

Inferring population demography and geographic connectivity in natural D. melanogaster populations using mitochondrial genome

Questions

  • Does spatial distance explain the variation in D. melanogaster mitochondrial genome?

  • How can we infer geographic connectivity between D. melanogaster populations?

Design and Method

Design and Method

Sampling

6 Locations 20 Samples

Outgroups:

2 Locations 5 Samples

Long Range PCR

Covering most of the genes on mtDNA

From ~1500 to ~13000

Sequencing

127 samples

Sample Processing

111 Samples

44 variant sites

54 haplotypes

Analysis

Population Genetic Analysis

Bayesian Methods with BEAST & BSSVS

To estimate potential migration events

Results: Relatedness

Bayes Factor Interpretation

BF Interpretation Supports
>100 Extreme support HA
30 to 100 Very strong support HA
10 to 30 Strong support HA
3 to 10 Moderate support HA
1 to 3 Anectodal support HA
=1 No evidence HA or H0
0.3 to 1 Anectodal support H0
0.1 to 0.3 Moderate support H0
0.03 to 0.1 Strong support H0
0.01 to 0.03 Very strong support H0
<0.01 Extreme support H0

Results: BSSVS

LOCATION Zambia Austria FL-Mia. MD-Chu. PA-Lin. PA-Ind. ME-Wel.
ME-Eustis 0.220 0.363 0.153 237.564 1.502 0.651 1
ME-Wells 0.440 0.186 0.186 21.381 0.09 0.29
PA-Indian 0.401 0.744 237.564 9.371 0.153
PA-Linvilla 0.121 237.564 0.121 0.401
MD-Churchville 237.564 4.639 1
FL-Miami 7.804 0.29
Austria 0.401

Summary

  • mtDNA is conserved in D. melanogaster, yet the diversity is not low.

  • Population structure

    • Cannot be explained by spatial distance between populations

  • Geographic connectivity in the mid- and long-range but not short-range

  • These methods can be used to infer migration rates between populations with temporal sampling.

Conclusion

Conclusion

  • Dynamically changing environments

  • Rapid adaptation

  • Prevalent views:

    • Migration is maladaptive
    • More variation is adaptive

  • The role of migration is context dependent

Acknowlegements

Advisor & Mentor
  • Paul Schmidt
Committee Members
  • Paul Sniegowski
  • Dustin Brisson
  • Mia Levine
  • Tim Linksvayer
Lab Members
  • Patricka Williams-Simon
  • Skyler Berardi
  • Jack Beltz
  • Hayes Oken
  • Edith Oteng
  • Caroline Barnhart
  • Charlie Pfeiffer
  • Winson Liu
  • Sekia Phillips

Previous Members

  • Seth Rudman
  • Evgeny Brud
  • Subhash Rajpurohit
  • Amy Goldfischer
  • Emily Behrman
  • Vinayak Marthur
Some Amazing Undergrads
  • Valentina Escudero
  • Yonatan Babore
  • Emma Torija
  • Ashleigh Williams
  • Liam Forsythe
  • Jordy Atencia
Collaborators and Funding sources

Brisson Lab

  • Matt Mitchell
  • Zach Oppler

Petrov Lab

Biology Department
  • Brian Gregory
  • Junhyong Kim
  • Dan & Winnie
  • Linda Robinson
  • Faculty
  • Staff
  • Housekeeping
  • Robin Sherwood
  • Leah Dennis
  • Colleen Gasiorowski
  • Ed Friess
  • Adam Linder

Thank you!