the population genetics of hybridization jonathan degner [email protected] 20 november, 2014

The population genetics of

hybridization

Jonathan Degner

[email protected]

20 November, 2014

Overview• What is hybridization?• Hybridization at a single locus• Hybridization at multiple loci• Quantitative traits• Epistatis

• Hybridization and fitness• Additive effects• Transgressive effects

• Summary

Jonathan DegnerPopulation genetics of

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What is hybridization?

“The crossing of individuals belonging to two unlike natural populations that have secondarily

come into contact”-Ernst Mayr, 1970


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Grammostola rosea Tamias striatus

x Tamiastola horrifadorablis


• Important in understanding many aspects of speciation • Reproductive isolation• Hybrid speciation• Interspecific gene flow

• Hybridization may refer to one of several different processes.

• May refer to first generation (F1) or advanced-generation (Fn)


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What is hybridization?• Secondary contact


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Time

Tem

pera

ture

What is hybridization?• Secondary contact


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Ancestral population Isolation Divergence Secondary contact

What is hybridization?• Intraspecific hybridization

• Gene flow between genetically distinct populations• Increases heterozygosity• Natural hybrids generally show intermediate phenotypes• Artificial hybrids may show transgressive phenotypes (e.g. maize)

• Interspecific hybridization• Gene flow between diverged species• Increases heterozygosity and can generate new polymorphisms• Hybrids may show intermediate, transgressive, or novel phenotypes


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What is hybridization?• Homoploid hybridization

• Does not result in a change in ploidy (e.g. 2N to 4N)• Generally less phenotypically pronounced than polyploidy

hybridization• Hybrids may be infertile or unfit due to differing chromosome numbers

between parents or epistatic interactions

• Polyploid hybridization• Ploidy in hybrids is higher than parents• Caused by fusion of non-haploid gametes• Hybrids may be infertile or unfit due to uneven ploidy or unusual

allelic effects


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Hybridization at a single locus


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Single locus


• For first-generation (F1) hybrids, genotype frequencies do not occur in Hardy-Weinberg equilibrium• If we are considering only hybrids, we are observing non-random

mating i.e. matings within populations are not being considered


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Single locus

Parent AA1 Aa1 aa1 AA2 Aa2 aa2

AA1 0 0.5 1

Aa1 0.5 0.5 0.5

aa1 1 0.5 0

AA2 0 0.5 1

Aa2 0.5 0.5 0.5

aa2 1 0.5 0


• If allele frequencies favor different alleles in two populations, hybrids will have “excess” heterozygosity i.e. > 0.5

• Taken to an extreme, populations with fixed differences will create fully heterozygous hybrids


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Single locus

F 1 h

eter

ozyg

osity

p1

p 2



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F 1 h

eter

ozyg

osity

p1

p 2

Hybridization at multiple loci


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Quantitative traits



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Quantitative traits

Trait value

Freq

uenc

y

Freq

uenc

yTrait value

Parent populations Offspring population



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Quantitative traits

Brennan et al. 2009

Parent populations Offspring population

Low variance High variance

• Hybridization may cause combinations of alleles across loci that have never been tested by selection, and may be deleterious.• Dobzhansky-Müller-Bateson incompatibilities

• Alleles that are co-adapted for local conditions can be broken up by gene flow and recombination• Outbreeding depression


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Hybridization at multiple lociEpistasis

• Dobzhansky-Müller-Bateson Incompatabilities


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IsolationNeutral mutation at separate loci

Secondary contactAncestral genotype

• Can result in hybrid sterility or low fitness

• Thought to be responsible for many speciation events• Orr and Turelli 2001


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Bomblies et al. 2007

Hybridization and fitness• Increased heterozygosity emphasizes selection on

heterozygous genotypes over the short term

• Additive phenotypes may be more fit in intermediate habitats (hybrid superiority) or universally less-fit (hybrid inferiority)

• Hybrids may exhibit transgressive phenotypes


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Hybridization and fitness


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Additive effects

Keim et al. 1989

• Hybrids are phenotypically intermediate between parents

• Most common outcome of hybridization due to the large number of genes typically involved in quantitative traits



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Additive effects

• In the habitat of parent population 1, we expect

parent1 > hybrid > parent2

• In the hybrid habitat, one of two scenarios can occur

parent1 < hybrid > parent2

parent1 > hybrid < parent2



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Hybrid superiority


• Common outcome of hybridization between populations with low to moderate divergence• Not enough time for

high levels of reproductive isolation to form

• Usually environment-dependent

Additive effects

Wang et al. 1997



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Hybrid superiority


• Can result in the formation of stable, extensive hybrid zones

• If hybrids are more fit over a large area, can result in the formation of “hybrid swarms”

Additive effects

De La Torre et al. 2014



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Hybrid superiority


• Allows species to colonize habitats that would otherwise be unavailable to them

• If hybrid populations become physically or reproductively isolated from parent populations, they may form a new species.

Additive effects



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Additive effects

Rushton 1978Po

llen

viab

ility

Species identity

Hybrids

Hybrid inferiority


• Common outcome of hybridization between populations with high divergence

• Usually environment-independent



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Additive effects

Hybrid inferiority


• Typically caused by epistatic interactions or the loss of phenotypes important for survival e.g. disease resistance

• Stable hybrid zones can still occur at an equilibrium between gene flow promoting hybridization and selection against it• Stable hybrid zones often appear as narrow bands between

two species’ range margins



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Parental sizes Offspring sizes

Facon et al. 2005

Transgressive effects

• Phenotype in hybrids is non-additive between parents

• Hybrids more likely to have higher or lower fitness than either parent

• May allow colonization of new habitats unavailable to either parent

Summary• Hybridization has profound effects at

allelic and phenotypic levels• Excess heterozygosity• New polymorphism• Increased genetic variance

• The overall outcome of hybridization on fitness is complex, difficult to predict, and often environment-specific• Additive fitness effects• Hybrid superiority/inferiority• Transgressive effects


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ReferencesBomblies, K., Lempe, J., Epple, P., Warthmann, N., Lanz, C., Dangl, J., and Weigel, D. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PloS Biology 5(9): e236.

Brennan, A., Bridle, J., Wang, A., Hiscock, S., and Abbott, R. 2009. Adaptation and selection in the Senecio (Asteraceae) hybrid zone on Mount Etna, Sicily. New Phytologist 183(3): 702-717.

De La Torre, A., Wang, T., Jaquish, B. and Aitken, S. 2014. Adaptation and exogenous selection in a Picea glauca x Picea engelmannii hybrid zone: Implications for forest management under climate change. New Phytologist 201(2): 687-699.

Facon, B., Jarne, P., Pointier, J., and David, P. 2005. Hybridization and invasiveness in the freshwater snail Melanoides tubercula: hybrid vigour is more important than increase in genetic variance. Journal of Evolutionary Biology 18(3): 524-535.

Keim, P., Paige, K., Whitham, T., and Lark, K. 1989. Genetic analysis of an interspecific hybrid swarm of Populus: Occurrence of unidirectional introgression. Genetics 123: 557-565.

Mayr, E. 1970. Populations, Species, and Evolution: An Abridgement to “Animal Species and Evolution”. Harvard University Press.

Orr, H. and Turelli, M. 2001. The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller incompatibilities. Evolution 55(6): 1085-1094.

Rushton, B. 1978. Quercus robur L. and Quercus petraea (Matt) Liebl: A multivariate approach to the hybrid problem. 1. Data acquisition, analysis and interpretation. Watsonia 21: 81-101.

Wang, H., McArthur, E., Sanderson, S., Graham, J., and Freeman, D. 1997. Narrow hybrid zone between two subspecies of big sagebrush (Artemesia tridentata: Asteraceae). IV. Reciprocal transplant experiments. Evolution 51(1): 95-102.


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Thank you for listening!

the population genetics of hybridization jonathan degner [email protected] 20 november, 2014

Documents

homoploid hybridization

single locus hybridization

heterozygosity natural

natural populations

contact ernst mayr

new polymorphisms hybrids

transgressive phenotypes

distinct populations