Coevolution• Fitness is a genotype-by-environment interaction.

• The environment for one species includes other species

• For species that interact, they form part of each other’s “environment”

• As one species adapts to the “environment” defined by the other species, the other species in turn can adapt to the changing “environment” created by evolution in the first species.

• Interactions between species therefore can set up an evolutionary feedback loop that causes the species to COEVOLVE in response to one another

Coevolution

Coevolution is simply natural selection

operating within each of the interacting species, recognizing that each

species constitutes part of the environment of the

other species.

Interspecific Interactions

Species 1 Species 2 Interaction

0 0 Neutralism

+ 0Commensalis

m

- 0 Amensalism

+ -Predator-prey;Herbivore-plantPathogen-host

- - Competition

+ + Mutualism

True Interactions

Predator-PreyE.g., HIV and Humans

Human Immune System and Cell Types Cause Selection On HIV v3 Region

Predator-PreyE.g., HIV and Humans

Does HIV Induce Natural Selection in Humans? If So, This Is A Co-Evolving System.

Predator-Prey

E.g., HIV and Humans

For HIV To Have An Impact on Human Evolution, This

Variation Must be Inherited (& Heritable)

There is much variation in the rate at which AIDS develops after HIV infection in humans, with some people never developing AIDS even decades after their original

infection.

Predator-Prey

E.g., HIV and Humans

Genome Scan For Resistance To HIV

Can Look For Evidence of Inheritance Through Linkage Analysis for QTL’s, With Locations Suggesting Candidate Genes

Predator-Prey

E.g., HIV and Humans

CCR5 As A Candidate Gene For Resistance to HIV

HIV-1 initially interacts with a cell-surface receptor, primarily CD4

Conformational changes in both the viral envelope and the CD4 receptor

permit the binding of gp120 to another cell-surface receptor, such as CCR5. HIV then fuses with the

cell.

People bearing a frameshift mutation in the CCR5 locus are resistant to HIV.

Under Isolation By Distance and Coalescent Theory, A New Mutant Is

Usually Most Frequent Near Its Center of Origin.

The CCR5 Frameshift Polymorphism

Coalescent Analysis Also Indicates Frameshift Mutant Originated 275-1,875

Years Ago.

The Current Allele Frequencies In Europe Are Too High To Have Evolved In This Time Period Under Genetic Drift (drift theory implies it would take about 127,000 years to explain its current European frequencies)

Hypothesis:

•The black plague bacillus produces an effector protein that binds CCR5 that leads to diminished immune response

•Europe has been subjected to several waves of black plague in the last 2000 years, including one that killed 25-33% of the population in 1346-1352

•CCR532 arose in Europe and could have been selected if it provides resistance to the black plague

Duncan, S. R., S. Scott, and C. J. Duncan. 2005. Journal Of Medical Genetics 42:205-208. Pop. gen. theory shows the plague could explain the current frequency

Sabeti et al. 2005. PLoS Biology 3.

Bollback et al. 2008. Genetics 179:497-502. Allele may be much older, so perhaps neutral evolution could explain it.

Zawicki, P., and H. W. Witas. 2008. Infection, Genetics and Evolution 8:146-151. Freq. of allele in bodies from 11-14th century Poland already at freq. of 5%, so either neutral or selection prior to Black Death.

Galvani and Slatkin. 2003. PNAS 100: 15276-15279. Poxviruses also use chemokine receptors, so perhaps evolved in response to smallpox, another potent selective agent in Europe and Western Asia (not mutually exclusive with role of plague as selective agent).

Subsequent Analyses

CCL3, CCL4, and CCL18 are potent chemoattractants produced by macrophages, natural killer cells,

fibroblasts, mast cells, CD4 + T cells, and CD8 + T cells. CCL3 and CCL4 are natural ligands for the primary human immunodeficiency virus type 1 (HIV-1) coreceptor CCR5 and are also known to

activate and enhance the cytotoxicity of natural killer cells.

Other Loci Have Been Identified For HIV Resistance via Candidate Locus Approach; e.g. Modi et al.

2006. Am J Hum Genet 79:120-128.

D in European Americans

Other Loci Have Been Identified For HIV Resistance via Genome Scanning and Candidate Loci Approaches, And Some Display Epistasis and Heterozygous Effects and High Allele Frequencies

(hence, they produce heritable variation).

SDF codes for a type of protein called a chemokine

that binds to other receptors used by HIV such as CXCR4, Causing the Receptor To Be Taken Into the Cell and No Longer on the Cell Surface

Current Statistics From South Africa

These differences in resistance translate into

heritable fitness differences, so HIV is affecting human evolution

Studies Are Now Underway To Identify Those Genes Subjected to Positive Selection In The Lineage Leading To

Humans. E.g., Vallender & Lahn (2004):

Function of Gene No. of Genes

Host-Pathogen Interactions

23

Reproduction 14

Sensory Systems 7

Dietary Adaptation 4

Neurotransmission 3

Brain Size & Anatomy

3

Skin Color 1

Other 8

COMPETITION

• Sometimes, one species out-competes competitors and drives them to extinction -- ends all coevolution

• Sometimes, coevolution results in adaptations that reduce competition such that the species can coexist.

The Finches of the Galapagos Islands

• Darwin found several species of closely related finches when he visited the Galapagos Islands.– The Galapagos Islands are very isolated so it is probable that these finches evolved from a common ancestor.

small groundfinch

large groundfinch

warbler finchtree finch using atwig to fish for insects

Competition in

Darwin’s Finches:

Beak Shape and Size Is

An Indicator of the

Types of Food The Birds Can

Eat.

h2 in G. fortis

Ancestral Reconstruction of Habitat Specialist

Evolution on Two Islands

TwigTrunk/Ground

Jamaica

Twig

Puerto Rico

Crown/Giant

Trunk/Ground

Crown/Giant

Trunk/Crown

Trunk/Crown

Grass/Bush

Crown

GeneralistGeneralist

Trunk/Grnd

Trunk/Grnd

MUTUALISM

E.g., Heliconius Butterflies

Heliconius erato

DifferentSpeciesIn TheSameArea

Heliconius melpomene

Heliconius melpomene

SameSpecies

InDifferentAreas

Baxter, S. W. et al. Genetics 2008;180:1567-1577

Heliconius melpomene and H. erato comimics

Passiflora

Heliconius caterpillars feed on passiflora, which makes them poisonous to birds. They evolve warning coloration. Experiments show that bird predators can quickly learn to avoid these color patterns, but this learning is more rapid when all butterflies in a single area converge upon a common pattern. This type of mutualistic mimicry is called Müllerian mimicry.

Heliconius cydno gathers pollen from Psiguria flower.

(Rainforest cucumber)

Coevolutionary interactions among

species can be complex;

e.g., Heliconius butterflies are

very long-lived as adults and reproduce

throughout that long life.

Therefore, they need a pollen source for

proteins. The species are involved in

intense competition for these pollen resources.

Different Heliconius species lay eggs on different species of Passiflora: are neutralists for larval

food resources

Different Heliconius species use the same pollen food resources: Hence their adult foraging

behaviors are driven by competitive interactions

Different Heliconius species are selected to converge upon a common, mutualistic warning coloration pattern by their interspecific

interaction with birds

Different traits within the same species can coevolve in radically different

directions. Mendelian genetics allows such complex coevolution to occur.

Mutualism

Competition

Neutralism

Mendelian genetics allows such complex coevolution to occur in part because

underlying genetics is simple.

Kronforst et al. (Genetics 174:535-539, 2006) did a genome scan using some of the most divergent species in genus. Found that different species achieved phenotypic convergence via homologous genes, and only 9 genes can explain the amazing wing diversity in this group.

Copyright © 2008 by the Genetics Society of America

Baxter, S. W. et al. Genetics 2008;180:1567-1577

Linkage maps comparing homologous chromosomes from H. erato, H. melpomene, and H. numata that affect red color shifts on wings

Baxter, S. W. et al. Genetics 2008;180:1567-1577

Analysis of recombinants spanning the HmB/D region on LG18

A methionine rich storage protein (MRSP) gene was identified, and comparative genetic mapping shows red wing color loci are in homologous regions of the genome of H. erato and H. melpomene. Subtle differences in these convergent phenotypes imply they evolved independently using somewhat different developmental routes, but are nonetheless regulated by the same switch locus.

Mendelian genetics allows such complex coevolution to occur in part because

underlying genetics is simple.

Reed RD, McMillan WO, Nagy LM (2007) Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proceedings of the Royal Society B: Biological Sciences 275, 37-45.

Coevolution Can Lead to Speciation (Kronforst et al. PNAS 103:6575-6580, 2006)

Interval MapOf MatingPreference

CompositeInterval Map

Of MatingPreference

0.05 Significance Threshold

H.c H.c H.p. H.p

H.c H.c H.p. H.p

Baxter, S. W. et al. Genetics 2008;180:1567-1577

Linkage map of H. melpomene LG18 (77.3 cM, log likelihood = -92.61)

Big Question: Why Do Any Species of Heliconius Have Regional Variation in Color Patterns? It Would Seem That A Single Universal Pattern Would Be The Most Effective Adaptive Solution.An Early Answer To This Was Pleistocene Refuges: the idea that climatic fluctuations in the Pleistocene created isolated subpopulations which adaptively diverged to form the initial “races”. Modern studies fail to support the existence of these refuges and modern comparative analysis indicate that the divergence times are not consistent with climatic fluctuations.

A second idea was that Heliconius species show strong population subdivision, and genetic drift interacting with selection (e.g., shifting balance) created differences among local populations leading to “races”. But modern population genetic studies indicate that most species of Heliconius are strong dispersers marked by much gene flow and little population subdivision.

They examined the fine-scale population genetic structure of eight Costa Rican Heliconius species with 1428 AFLP markers. The species were chosen from two clades: molecular phylogenetics indicates that one clade was the first to diversify into local “races”, and the second clade evolved later to parallel the first group through coevolution.

Kronforst and Gilbert (2008, Proceedings of the Royal Society B: Biological Sciences 275:493-500) suggest an alternative.

Large fst,

Sign. IBDSign. IBD

Sign. IBD

3 of the 4 species in the older clade show significant isolation by distance, and the most abundant species (H. erato), which should dominate much of the coevolution, has a large fst, indicating a strong potential drift and shifting balance.

The species in the clade that later radiated onto these patterns had intermediate levels of genetic diversity and less genetic differentiation among populations.

Kronforst and Gilbert (2008, Proceedings of the Royal Society B: Biological Sciences 275:493-500) suggest an alternative.

Sign. IBDOnly 1 of the 4 species in the younger clade show significant isolation by distance: little potential for drift and shifting balance.

Genetic Drift in perhaps just one, widespread, abundant but highly subdivided species triggered adaptive local

differentiation in other species through coevolution that did have the population structure to initiate such

differentiation.