Genomics of speciation and adaptation: Local adaptation & Ecological speciation

12.03.2019, Filip Kolář Where we are today?

The gray zone of speciation

Potential for gene flow is decreasing … reproductive isolation is accumulating Big question in this early phase

What is the role of selection in speciation?

 Ecological triggers?  Ecological speciation (link divergent selection & reproductive isolation)  What makes the BDMI to arise – drift vs. selection?

Sympatric speciation? (not today)

Genomic architecture of early speciation  Islands of divergence (not today) Adaptation

A feature of an organism that has been favoured by natural selection because its positive effect on relative fitness Local adaptation

 Trait conferring higher fitness in specific environmental conditions (e.g. saline, serpentine soil, alpine env.)  Adaptations are local – not found throughout species’ range  Result of divergent selection   Strict definition: Higher fitness at native site than any other introduced population Local adaptation

 Wild mice (Petromyscus) on differently coloured substrate          Arabidopsis thaliana in Italy vs. Sweden Local adaptation

 Strict definition: Higher fitness at native site than any other introduced population

Local Local Local

Local

Local Local

Local Local

Which of these show local adaptation (after L. Rieseberg) Ecotype

A genetically distinct population/lineage adapted to specific local conditions

Betula in Uppsala (Turesson 1930)

Achillea in Sierra Nevada (Clausen, Keck Hiesey 1948) Side-note: Adaptive plasticity

Plastic response on its own is adaptive (Not regarded here)

Ranunculus subg. Batrachium – Terrestrial vs. aquatic form Why study local adaptation Evolutionary biology - quantifying selection strength “real-time” (ecological time) - may be incipient speciation - maintains genetic variation within a species

Broader Impact - response to environmental change (immobile plants!!) - agriculture, forestry, human health

Tree provenance trial

Humans (Fan et al. 2016 Science) How study? Reciprocal transplant experiment

Genetic differentiation for traits related to fitness - suggests local adaptation

Arabidopsis thaliana in Sweden Peromyscus enclosures in Nebraska How study? Reciprocal transplant experiment How to measure fitness? Biomass?

Recruitment / Survival

N of progeny (and their fitness?)

Among-year variation Agren Schemske 2012 New Phytol. Hereford 2008 How study? Environmental clines Clinal variation – altitudinal, latitudinal gradients Generality?

50 - 71% of cases – LA detected 45% average relative home-advantage

Stronger LA  Larger env. differences  Larger populations

Hereford 2008 (74 plant & animal studies), Leimu & Fischer (2008) (35 plant studies) Trade-off?

Costs in the non-native environment?

Hereford 2008 Genetic basis & genomic architecture Environmental association Common gardens studies

NonsynSNPs (red) Syn. (green) LA-associated alleles – original sampling spots intergenic (yellow) associated with climate Hancock et al. 2011 Science, Fournier – Level et al. 2011 Science

Genetic mapping (e.g., QTL): Cross both pops – subject F2 mapping population to both environments → “fitness loci” Genomic architecture? Generally largely unknown

Differing fitness optima

Few large-effect loci

Many small-effect loci

Lascoux et al. 2016 Genomic architecture?  A. thaliana cross+RILs   Few (15) fitness QTLs  1/3 of them trade-offs (local genotype favoured at each site)  SW: freezing tolerance IT: flowering time

Agren Schemske 2012 New Phytol.

15 Fitness QTLs (5 with trade-offs) in Arabidopsis thaliana, 398 RILs, 3 years, 40,000 plants (Agren et al. 2013 PNAS) Genetic basis?

Genetic basis of fitness trade-offs:

 Genetic trade-off – allele beneficial at A, negative at B

 Conditional neutrality – allele beneficial at A, neutral elsewhere

Two loci affecting the same fitness trait (Savolainen et al. 2013) Genomic architecture? Flowering time  Conditional neutrality (beneficial in Italy, neutral in Sweden)

Flowering time QTLS and overlap with fitness trade-off QTLs (arrow) (Agren et al. 2016 Evolution) Adaptation genes? Peromyscus: Local adaptation (evolution experiment) … at which site is selection stronger?

Environment Survival Shift in Barrett et al. 2019 Science coloration Adaptation genes? … and the Agouti locus

Allele freq. Change (recapture exp.) – significant in 549 SNPs ENCLOSURE

WILD POP.

Divergence scan – among SNPs associated with colour: single AA deletion significant selection signal (in both enclosure and natural pop) Mus transgenics … link: genotype-phenotype-fitness Wildtype Serine KO Barrett et al. 2019 Science Limits to adaptation

No genetic variation

Drift (can oppose selection)

Fluctuating selection (in time)

Gene flow (still LA possible, will prefer fewer loci with large effects)

Savolainen et al. 2013 Adaptation or relaxed constraint? Is the alpine smaller because was selected for (freezing) or just mutation was tolerated (no competition)?

Arabidopsis thaliana in ~4000 m a.s.l. Limits to adaptation - constraints Genetic correlations among traits (e.g. pleiotropy) (modified after L. Rieseberg) • Imagine a case where a single diallelic locus controls both inflorescence height and date of first flower Positive genetic Short inflorescence correlation t

h 40 g i

A e 35 h

e 30 a

c NS

Early flowering n

e 25 c

s 20 Tall inflorescence e NS r o

l 15 f

n A a I 10 6 11 16 21

Late flowering Flowering date

• Can natural selection lead to late flowering plants with short inflorescences? • Can natural selection lead to early flowering plants with tall inflorescences? Limits to adaptation - drift

Small populations

When migration – selection balance each other

(Yeaman & Otto 2011, Lascoux et al. 2016) Ecological speciation

When local adaptation turns into speciation…

Wider definition: speciation triggered by divergent selection

Three components:

 Ecological source of divergent selection

 Reproductive isolation

 Genetic component linking the two above

Nosil 2012 Ecological speciation

When local adaptation turns into speciation…

 Shared genetic mechanism

Nosil 2012 Ecological speciation

Timema cristinae stick insect in California

 Camouflage mechanisms – these loci resist introgression (accenuated differentiation between races)  But does not affect mate-choice – instead assoc. with affected polygenic chemical signals (not growth of peaks of divergence) Timema bartmani

Genetic diff. In Timema cristinae (Riesch et al. 2016 Nature Ecol Evol) Ecological speciation – key question

How the gene flow is restricted?

 Allopatry

 Sexual selection

 Reinforcement

 “Magic traits” - one gene - pleiotropy on RI and target of divergent selection Ecological speciation – key question

How the gene flow is restricted?

 “Magic traits” - one gene - pleiotropy on RI and target of divergent selection

Wing colour patterns (mating pref. incl. paper models & divergent sel.) (Jiggins et al. 2001 Nature) Ecological speciation – key question

What is the genetic basis?  The same locus?  Mimulus guttatus – copper mine adaptation

 Copper adaptation and hybrid lethality – two tightly linked loci → hitchhiking of the RI allele

Segregating (C) and non-segregating (D) F2 indivs for copper tolerance (Copperopolis allele of Tol gene) (Wright et al. 2013 Plos Biology) Ecological speciation

 Ecological source of divergent selection  Environmental differences  Sexual selection  Ecological interactions (e.g. plant-pollinator)

 Reproductive isolation  Habitat and temporal isolation (flowering time)  Immigrant inviability  Sexual /pollinator isolation  Postzygotic isolation (intrinsic, ecological, sexual)

 Genetic component linking the two above  Direct selection & Pleiotropy  Indirect selection & Linkage Gene flow

Things might get more complex…  Selection acting on constraints for speciation

Melanistic form of Timema cristinae acts as a bridge in gene flow (Comeault et al. 2015 Curr.Biol.)