EcologicalEcological andand EvolutionaryEvolutionary Genetics:Genetics: PartPart 2 FSFS 20102010

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University of Basel, 09.03.2010

Evolution by natural selection

Charles Darwin Alfred Russel Wallace

1 NaturalNatural diversitydiversity asas wewe directlydirectly observeobserve itit isis „phenotypic“„phenotypic“

NaturalNatural selectionselection actsacts onon phenotypesphenotypes

EvolutionaryEvolutionary changechange onlyonly occursoccurs ifif phenotypesphenotypes areare passedpassed onon toto nextnext generationgeneration (heritable)(heritable)

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Darwin‘sDarwin‘s and and Wallace‘sWallace‘s theorytheory of of EvolutionEvolution byby Natural Natural Selection Selection requires requires a a mechanismmechanism of of traittrait inheritance inheritance across across generations.generations. Darwin,Darwin, withoutwithout knowledge knowledge ofof Mendel‘sMendel‘s experiments, experiments, assumedassumed some some obscureobscure blending blending mechanism mechanism („pangenesis“).(„pangenesis“).

Pangenesis: body cells shed „gemmules“, which collect in the reproductiv organs prior to fertilization.

2 Jean-BabtisteJean-Babtiste LamarckLamarck 18091809.. PhilosophiePhilosophie ZoologiqueZoologique;; firstfirst fullyfully formulatedformulated evolutionaryevolutionary ttheoryheory („transmutation(„transmutation ofof thethe species“)species“) basedbased onon thethe assumptionsassumptions thatthat EvolutionEvolution „aims“„aims“ at at higherhigher developmentdevelopment andand complexicomplexity,ty, andand thatthat traittrait inheritanceinheritance isis basedbased onon acquiredacquired variationvariation

CharlesCharles DarwinDarwin && Alf Alfredred RusselRussel Wallace.Wallace. 1858 1858.. OnOn thethe tendencytendency ofof speciesspecies toto formform varieties;varieties; andand onon thethe perpetuationperpetuation ofof varietiesvarieties andand spspeciesecies byby naturalnatural meansmeans ofof selectionselection.. JournalJournal ofof thethe ProceedingsProceedings ofof thethe LinnLinneanean SocietySociety ofof LondonLondon 3,3, 46-50.46-50. (Darwin:(Darwin: essayessay fromfrom 1844.1844. ExtractExtract fromfrom anan unpublishedunpublished workwork onon speciesspecies;; Wallace:Wallace: essayessay fromfrom 1958.1958. OnOn thethe tendencytendency ofof varietiesvarieties toto departdepart infiniteinfinitelyly fromfrom thethe originaloriginal typetype))

CharlesCharles Darwin.Darwin. 18591859.. TheThe originorigin ofof speciesspecies byby meansmeans ofof naturalnatural selectionselection.. JohnJohn Murray,Murray, London.London.

Gregor Mendel. 1866. Versuche über Pflanzenhybriden. Mitteilung in: Verhandlungen des naturforschenden Vereines in Brünn (pp. 3-47).

705:224 Gregor Mendel (1822-1884) (3.15 : 1) Pisum spp.

3 “The“The variousvarious formsforms ofof PeasPeas seselectedlected forfor crossingcrossing showedshowed differencesdifferences inin lengthlength andand colorcolor ofof thethe stem;stem; inin thethe sizesize andand formform ofof thethe leaves;leaves; inin thethe posposition,ition, color,color, sizesize ofof thethe flowers;flowers; inin thethe lengthlength ofof thethe flowerflower stalk;stalk; inin thethe color,color, form,form, andand sizesize ofof thethe pods;pods; inin thethe foformrm andand sizesize ofof thethe seeds;seeds; andand inin thethe colorcolor ofof thethe seed–cseed–coatsoats andand ofof thethe albumenalbumen (endosperm).(endosperm). SomeSome ofof thethe charcharactersacters notednoted dodo notnot permitpermit ofof aa sharpsharp andand certaincertain separation,separation, sincesince thethe differencedifference isis ofof aa “more“more oror less”less” nature, nature, whichwhich isis oftenoften difficultdifficult toto define.define. SuchSuch characterscharacters couldcould notnot bebe utilizedutilized forfor thethe separateseparate experiments;experiments; thesethese couldcould onlyonly bebe appliedapplied toto characterscharacters whichwhich standstand outout clearlyclearly andand defdefinitelyinitely inin thethe plants.plants. ““ (Mendel,(Mendel, G.G. 1966)1966)

→ Mendel actively selected discontinuous traits.

CharlesCharles Darwin.Darwin. 1968.1968. TheThe variationsvariations ofof animalsanimals andand plantsplants underunder domestication.domestication. (the(the „pangenesis„pangenesis book“)book“)

DarwinDarwin couldcould havehave (re-/co-)(re-/co-) discovereddiscovered Mendel‘sMendel‘s laws,laws, butbut despitedespite extensivextensivee breedingbreeding experiments,experiments, hehe nevernever diddid thethe criticalcritical crossescrosses thatthat couldcould havehave revealedrevealed MendelianMendelian 3:13:1 ratiosratios ofof phenotypes.phenotypes. DarwinDarwin waswas aimingaiming atat cconfirmingonfirming his pangenesis theory,theory, andand anotheranother focusfocus in hishis breedingbreeding experimentsexperiments waswas onon inbrinbreedingeeding andand heterosisheterosis effects.effects.

4 Darwins crossing experiments (The variations of animals and plants under domestication, 1868) (The effects of cross- and self-fertilization in the vegetable kingdom, 1876)

57 Arten, 51 Gattungen, 30 Familien

→ Darwin focussed on continuous traits (e.g. stem length).

Hugo de Vries, Carl Cohens, Erich Tschermak. Early 20th century: Independent rediscovery of Mendel‘s laws.

Carl Correns. 1900. G. Mendels Regel über das Verhalten der Nachkommenschaft der Rassenbastarde, Berichte der Deutschen Botanischen Gesellschaft 18 (1900), 158-168.

“The latest publication of Hugo de Vries: Sur la loi de disjonction des hybrides which through the courtesy of the author reached me yesterday, prompts me to make the following statement: In my hybridization experiments with varieties of maize and peas, I have come to the same results as de Vries, who experimented with varieties of many different kinds of plants, among them two varieties of maize. When I discovered the regularity of the phenomena, and the explanation thereof –– to which I shall return presently –– the same thing happened to me which now seems to be happening to de Vries: I thought that I had found something new.2 But then I convinced myself that the Abbot Gregor Mendel in Brünn, had, during the sixties, not only obtained the same result through extensive experiments with peas, which lasted for many years, as did de Vries and I, but had also given exactly the same explanation, as far as that was possible in 1866.

5 A History of Quantitative Genetics II havehave nono patiencepatience withwith thethe hypothesishypothesis occasionallyoccasionally expressed,expressed, andand oftenoften implied,implied, especiallyespecially inin talestales writtenwritten toto teachteach childrenchildren toto bebe good,good, thatthat babiesbabies areare bornborn prettypretty muchmuch alike,alike, andand thatthat thethe solesole agenciesagencies inin creatingcreating differencesdifferences betweenbetween boyboy andand boy,boy, andand manman andand man,man, areare steadysteady applicationapplication andand moralmoral effort.effort. ItIt isis inin thethe mostmost unqualifiedunqualified mannermanner thatthat II objectobject toto pretensionspretensions ofof naturalnatural equality.equality. TheThe experiencesexperiences ofof thethe nurnursery,sery, thethe school,school, thethe Francis Galton: Victorian polymath: University,University, andand ofof professionalprofessional careers,careers, areare geographer, meteorologist, tropical aa chainchain ofof proofsproofs toto thethe contrary.contrary. explorer, founder of differential ---- Francis Francis GaltonGalton (1869),(1869), HereditaryHereditary psychology, inventor of fingerprint GeniusGenius identification, pioneer of statistical correlation and regression, inventor of the Quincunx, convinced hereditarian, eugenicist, half-cousin of Charles Darwin.

Galton‘sGalton‘s 22 (wrong)(wrong) interpretations:interpretations: nono evolutionevolution duedue toto 1)1) Lack Lack ofof mechanismmechanism leadingleading toto changechange inin traittrait meanmean 2)2) „ „regressionregression toto mediocritymediocrity (mean)“(mean)“ andand thethe resultingresulting lossloss ofof heritableheritable variationvariation 1886 Arnold 1994

6 Solution to problem 1)

1903

Solution to problem 2)

• G. H. Hardy and Wilhelm Weinberg (1908): independently proved that stable genetic polymorphisms can be maintained in populations in the absence of selection. The „Hardy-Weinberg law“ solved the paradox of „regression to the mean“ once it was acknowledged that continuous variation is based on the segregation of many loci. But this is what Mendelians and biometricians could not agree on for long time. Male gamet A(p) a(q)

2 2 A(p) AA(p2) Aa(pq) p + 2 pq + q =1 p + q =1

a(q) aA(pq) aa(q2) Female gamet

7 Mendelians Biometricians (early geneticists)

3:1 F2 ratios

Lynch & Walsh 1998

Mendelians Biometricians

LeadLead by by LeadLead by by WilliamWilliam BatesonBateson KarlKarl PearsonPearson W.W. F.F. R.R. WeldonWeldon

EvolutionisdrivenbyEvolutionisdrivenby EvolutionEvolution is is the the result result of of variationvariation in in discretediscrete naturalnatural selection selection acting acting upon upon characterscharacters that that arise arise by by continuouslycontinuously distributed distributed macromutationsmacromutations.. No No rolerole forfor characterscharacters.. Inheritance Inheritance is is selection.selection. InheritanceInheritance is is assumedassumed to to bebe based based on on assumedassumed to to bebe based based on on somesome blending blending mechanism. mechanism. single-locussingle-locus effects. effects.

8 • Swedish geneticists H. Nilsson-Ehle provides support for the „multiple factor hypothesis“ from crossing experiments with various cereal crops in 1909. Cross-breeding among inbred strains results typically in an outburst of trait variation among F2 offspring (Sidenote: Darwin had done similar experiments, but he stopped at F1). Similar results from experiments by East (1911) on corn ear size („Ähren-Grösse“)

F0 (2 inbred lines)

F1-cross

F2-cross

9 • Danish botanist Wilhelm Johannsen (1903, 1909) identified environmental influences on trait expression, and coined the terms „genes“, „genotype“ and „phenotype“.

• The dispute between Mendelians and Biometricians seemingly resolved by the developments during the „Modern Synthesis“ (J. Huxley), the topic would result in a new fierce scientific/public debate in the 70ies with a somewhat different angle: the Nature-Nurture debate between behaviorists and behavior geneticists.

• Some of the original debate (macro-mutation versus selection on continuously variable traits underlying evolutionary change) is still visible in the more recent literature. Also, there is frequent disagreement (or maybe rather misunderstanding) between molecular and evolutionary biologists.

10 Summary: From Mendelian to quantitative genetics

1. Shift from individuum to population 2. Single individuum is not informative, only patterns of differences among individuals allow us to interpret phenotypes • E.g., eye colour or blood group can be used for paternity-identification of individual offspring • Body size or hair colour not very useful to this end 3. Shift from gene-frequencies to gene effects and components of genetic and environmental variation that define phenotypic differences between individuals within (and/or among) populations

„Side-effects“ of the development of an inheritance theory based on the resemblance among relatives

Fundaments for regression and Francis Galton correlation analysis, etc.

Mathematically explicit correlation Karl Pearson methods, regression methods, hypothesis testing, etc.

Analysis of variance (developed for the Ronald A. Fisher purpose of sib-sib analyses), variance components, maximum likelihood, hypothesis testing, etc.

Sewall G. Wright Statistical path analysis,

Foundation of modern statistical methodology

11 A formal theory of quantitative genetics: animal breeding and evolution

A formal theory of quantitative genetics: animal breeding and evolution

Chapter one Variation under domestication Chapter two Variation under nature

Darwin, C. 1859. The origin of species. John Murray

Darwin, C. 1968. The variations of animals and plants under domestication. John Murray

12 The integration of the formal quantitative genetic theory into an evolutionary framework was largely due to Russell Lande, Jim Cheverud, Stevan Arnold, Mark Kirkpatrick (in the 70ies through 90ies), and others.

Evolutionary Quantitative Genetics

PhenotypicPhenotypic evolutionevolution == selectionselection ** inheritedinherited variancevariance

Premise: the study of phenotypic evolution does not require detailed understanding of molecular mechanisms underlying its expression

13 Selection = phenotype-fitness covariance

FITNESS Evolutionary Ecology

Sociobiology

Behavioral Ecology

Phenotype- Fitness Covariance Demography

Reproductive biology

Inheritance = phenotype-genotype covariance

Functional Genomics

Endocrinology

Developmental Biology

Phenotype- Genotype Physiology Covariance Psychology

14 The quantitative genetic approach

StatisticalStatistical approximationapproximation basedbased onon differencesdifferences inin individualsindividuals ofof populations.populations. FocusFocus on componentscomponents ofof variationvariation Phenotype- Genotype thatthat areare importantimportant forfor Covariance explainingexplaining phenotypicphenotypic evolutionevolution

Rhombus

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