The relative role of drift and selection in life-history The relative role of drift and selection in life-history evolution: a case study from recently founded evolution: a case study from recently founded

populations of graylingpopulations of grayling

Mikko Koskinen, Thrond Haugen & Craig PrimmerMikko Koskinen, Thrond Haugen & Craig Primmer

Outline

• Background to ‘Darwinian’ vs ‘neutral’ evolutionary theories

• Presentation of the framework of this studyPresentation of the framework of this study

• Results and conclusionsResults and conclusions

Natural Selection vs Random Drift?Natural Selection vs Random Drift?

• Transplantation experiments suggest that selection is an Transplantation experiments suggest that selection is an efficient evolutionary forceefficient evolutionary force

-- Anolis Anolis lizards were lizards were introduced onto small islandsintroduced onto small islands

- Populations differentiated from - Populations differentiated from each other over 10-14 years accordingeach other over 10-14 years accordingto the recipient island’s vegetationto the recipient island’s vegetation

(Losos (Losos et al.et al. 1997, 1997, NatureNature))

• Comparisons of phenotypic differentiation and selectively Comparisons of phenotypic differentiation and selectively neutral differentiation (e.g. from non-coding DNA neutral differentiation (e.g. from non-coding DNA microsatellites) suggest that selection is an efficient microsatellites) suggest that selection is an efficient evolutionary forceevolutionary force

QQST

FFST

0.010.01 0.10.1 110.010.01

0.10.1

11

-- Mean quantitative genetic (Mean quantitative genetic (QQSTST))

differentiation generally exceededdifferentiation generally exceededneutral marker gene (neutral marker gene (FFSTST) differentiation) differentiation

(Merilä & Crnokrak 2001, (Merilä & Crnokrak 2001, J. Evol. Biol.J. Evol. Biol.))

Natural Selection vs Random Drift?Natural Selection vs Random Drift?

• In stark contrast with the Darwinian view, influential In stark contrast with the Darwinian view, influential theories (e.g. Wright 1931, Kimura 1995) suggest that drift theories (e.g. Wright 1931, Kimura 1995) suggest that drift is the dominant evolutionary force in finite populationsis the dominant evolutionary force in finite populations

• It is fair to say that the ‘neutral drift hypothesis’ has been It is fair to say that the ‘neutral drift hypothesis’ has been among the most controversial issues in evolutionary biology among the most controversial issues in evolutionary biology in the last 50 years, and is empirically understudiedin the last 50 years, and is empirically understudied

S. Wright

Natural Selection vs Random Drift?Natural Selection vs Random Drift?

Outline

• Background to ‘Darwinian’ vs ‘neutral’ evolutionary Background to ‘Darwinian’ vs ‘neutral’ evolutionary theoriestheories

• Presentation of the framework of this studyPresentation of the framework of this study

• Results and conclusionsResults and conclusions

Norway

Study system

European grayling,Thymallus thymallus

The ‘plan’

• To measure quantitative genetic differences (QST) between the populations using ‘common-garden’ experiments (six early life-history traits)• Three temperatures, three populations with half-sib design

• Four unique females mated with each male (28 families per population)

(Spitze et al 1993, Genetics)

Variance components from mixed-model Anova

95% CI from non-parametric bootstrapping

• To measure neutral genetic differences (FST), i.e. the effect of drift, using 17 microsatellite DNA loci

22

2

2 GWGB

GBSTQ

The ‘plan’

• To investigate the demographic history of the populations using microsatellites, and to use that for interpreting how the results relate to the ‘Darwinian’ vs ‘neutral’ evolutionary theories

• To test the null-hypothesis of neutral evolution of the six traits using:

(Lande 1976, Evolution)

-Ne = effective population size (maximum-likelihood estimate from microsatellite data)

-2GB = additive genetic variance between populations

-2GW = additive genetic variance within populations (among sire var comp)

-h2 = narrow-sense heritability in a given population and environment

-t = divergence time of populations

th

NF

GW

GBe22

2

,1

Outline

• Background to ‘Darwinian’ vs ‘neutral’ evolutionary theories

• Presentation of the framework of this study

• Results and conclusionsResults and conclusions

Results - neutrality tests

• Neutral evolution was rejected for the majority of the trait• Recall:

Trait F P

length at termination 384 <0.0001

yolk-sac volume 647 <0.0001

growth rate 111 <0.0001

incubation time 17.4 <0.0001

swim-up length 2.50 0.1235

hatching length 0.70 0.5472

th

NF

GW

GBe22

2

,1

Trait F P Ne(sign)

length at termination 384 <0.0001 0.25

yolk-sac volume 647 <0.0001 0.14

growth rate 111 <0.0001 0.84

incubation time 17.4 <0.0001 5.33

swim-up length 2.50 ns 37.1

hatching length 0.70 ns 218

Results - neutrality tests

• Extremely low Ne estimates, not compatible with sexual reproduction, would have been required for drift to dominate over selection

F1, = 3.84 for P 0.05

Results - QST vs FST

• Population differences based on quantitative traits (QST) often strikingly exceeded the analogous measures based on microsatellites (FST)

FST

length at termination

yolk-sac volume

growth rate

incubation time

swim-up length

hatching length

Les vs Ht

0.0 1.00.5

Results - demographic history

• Effective sizes of the populations were small

• Microsatellite diversity within populations was low• The populations have historically experienced severe

‘bottlenecks’

Population n Ne (95% CI) A (SD) N0 / N1 (95% CI)

Les 52 88.9 1.9 (1.1) 0.003 (0.0003-0.03)

Ht 48 24.2 (12.1-42.2) 1.5 (0.9) 0.006 (0.0003-0.05)

ØM 49 85.0 (36.0-170.5) 1.7 (0.9) 0.0006 (0.00008-0.01)

Aur 28 55.4 (24.8-110.0) 1.6 (0.9) 0.001 (0.0003-0.005)

Show examples of Ne sampling distributions and likewise for N0/N1

Conclusions

• The evolution of the phenotypic differences between the populations was dominantly due to natural selection

-neutrality tests [F-test and Ne(sign) estimates]-QST vs FST comparisons

• Provide Fst/Qst+Fst

• However, also drift had a notable effect (FST = 0.05-0.21)

• The dominating effect of selection is interesting in the light of the demographic history of the populations.

• According to the influential ‘neutral theory’, the low Nes and bottlenecks should have emphasized the effect of drift

Conclusions

Acknowledgements

• Thanks to Juha Merilä, Mark Beaumont, Asbjørn Vøllestad, Peter Crnokrak, Andrew Hendry, Martin Lascoux and Nick Smith for helpful comments!