Adaptation and genetics. Block course Zoology & Evolution 2013, Daniel Berner
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1 Adaptation and genetics Block course Zoology & Evolution 2013, Daniel Berner 2
2 Conceptual framework Evolutionary biology tries to understand the mechanisms that lead from environmental variation to biological diversity Environmental contrast Divergent natural selection Adaptive diversification Performance Savanna Body size Trees Color Ecology Genetics 3
3 Goal of the lecture Introduce methods for the investigation of adaptive diversification among groups of organisms: 1. Phenotype-environment association 2. Transplant approaches 3. Direct study of evolution 4. Ecological genome scans Illustrate applications of these methods in threespine stickleback fish, a powerful evolutionary model organism 4
4 1. Phenotype-environment association The consistent association of a trait with a specific habitat type can provide good evidence of adaptation and shed light on the ecological cause of selection This association can occur at different taxonomic levels Environment A Environment B Environment A Environment B Environment B Environment A 5
5 Example: convergent evolution in threespine stickleback Stickleback have repeatedly colonized freshwater habitats from the ocean (ancestral habitat) Dario Moser 6
6 Divergence of freshwater stickleback into two distinct foraging (resource) niches Limnetic (open water) prey Benthic (bottomdwelling) prey Stomach content analysis in eight lake-stream population pairs, Vancouver Island, Canada Divergence in resource use is predictable; similar trends in Canada and Europe Mean proportion of limnetic prey (+SE) L S Berner et al Be Bo Jo Mc Mi Mo Py Ro Lake-stream system 7
7 Phenotype-environment association: predictable trait shifts between limnetic and benthic-foraging stickleback types Enos lake Limnetic type Benthic type Berner et al Limnetic type Benthic type Gill rakers Robert s lake-stream 8
8 Analysis of shape and gill rakers along replicate lake-stream gradients Vancouver Island Berner et al Ireland Ravinet et al
9 Example: convergence at higher taxonomic level Similar phenotype-environment association in distantly related fish species (stickleback and whitefish) Kahilainen et al
10 Summary Stickleback divergence into benthic and limnetic foraging niches coincides with predictable shifts in body shape and gill raker morphology This divergence has evolved multiple times independently in freshwater following the colonization by ancestral marine stickleback Similar morphological divergence is observed in distantly related fish groups showing the same specialization in resource use Strong evidence that divergence is adaptive Studies on phenotype-environment associations are relatively easy to carry out and cheap Correlational, and no information on the genetic basis 11
11 2. Transplant approaches Raising populations in new environments and studying their fitness and phenotypes can inform on adaptive divergence and shed light on its genetic basis Environment A Environment B Environment A Environment B Environment C 12
12 Reciprocal transplant experiment: raising populations (and optionally their hybrids) in their native and in foreign environments ( at home and away ) Environment A Environment B Measuring fitness (or correlates) at home and away informs on the presence and strength of divergent selection and local adaptation Fitness A B A B Natives outperform foreigners evidence for divergent selection A-type always outperforms B-type no evidence for divergent selection 13
13 Measuring traits at home and away informs on the relative importance of genetic versus environmental ( plastic ) contributions to phenotypic population divergence Trait value A B A B Trait values are independent from the environment population differentiation is mainly genetic Trait values depend strongly on the environment - population differentiation is due mainly to phenotypic plasticity 14
14 Common garden experiment: raising populations (and optionally their hybrids) in a common, controlled environment Environment A x Environment B Common garden Allows testing for a genetic component to phenotypic diversification seen in nature. Can inform on the mode of inheritance if hybrid lines are inlcuded ( line cross analysis ) Trait value A In nature B Trait value Common garden Trait value Common garden Differentiation in nature is non-genetic Genetic differentiation with dominance 15
15 Examples Reciprocal transplant: detecting divergent selection in a benthic-limnetic stickleback pair (Schluter 1995; Hatfield & Schluter 1999) Reciprocal transplant of juvenile stickleback to littoral and open water cages in Paxton Lake, Canada Growth (fitness correlate) measured after 3 weeks Local adaptation: at home, each type outperforms the other Hybrids perform poorly in both habitats 16
16 Common garden: investigation of the inheritance of foragingrelated traits by line cross analysis in lake-stream stickleback (Berner et al. 2011) Raising Misty lake and stream stickleback, and derived hybrid cross lines, under laboratory common garden conditions over 3 generations Measurement of ecologically important morphological traits Genetic differentiation; genetic factors are additive Genetic differentiation; genetic factors show strong dominance 17
17 Common garden lab study with experimental treatments: does phenotypic plasticity facilitate the colonization of new habitats? (Wund et al. 2008) Raising juvenile stickleback from 3 Alaska populations under 2 experimental conditions (limnetic and benthic diet) Measurement of phenotypes believed to be ecologically important limnetic marine benthic limnetic benthic marine Weak phenotypic plasticity; differentiation is largely genetic Plastic response can be population-dependent 18
18 Summary Population divergence in stickleback foraging-related morphology has a genetic basis Genetic architecture likely differs between traits (although these approaches cannot lead us to genes) This divergence seems to contribute to local adaptation Transplant approaches are typically highly labor-intensive; sometimes very difficult to carry out in the wild 19
19 3. Direct study of evolution Tracking phenotypes over time can allow observing adaptation in action, and can shed light on its ecological cause A precondition is that the study population harbors genetic variation in the trait(s) under selection Generation 0 Generation 1 Generation 2 20
20 Selection experiments may involve tracking a phenotype after the exposure to novel a environment (in the wild or lab)... Environment A Environment B G 0 G 1... or may track phenotypic change in natural situations (for example, where populations receive immigrants) Environment A Environment B 21
21 Example: lateral plate evolution in stickleback Lateral plates (derived from scales) serve as armor in stickleback exposed to predation by larger fish Cresko et al Completely plated morph (typical of ancestral pelagic life style) Low-plated (derived) morph (common in derived freshwater populations) Colonization of Loberg Lake (Alaska) by marine stickleback; tracking of plate morph frequencies Bell et al
22 Studying lateral plate evolution at the gene level Identification of Ectodysplasin as a major determinant of plate morph by using QTL mapping (see Dieter Ebert s lecture) Colosimo et al Selection experiment: release of heterozygous individuals from the ocean to freshwater ponds Barrett et al Tracking of Ectodysplasin genotypes over one year 23
23 Summary Direct evidence of rapid adaptive evolution in lateral plates upon freshwater colonization Despite an overall life-time benefit of the low-plated allele in freshwater, selection seems life-stage specific General ecological context known, but the exact mechanistic cause of selection remains uncertain Unless the genetic basis of divergence is already known, evolution experiments tell us little about genetics 24
24 4. Ecological genome scans When selection drives frequency shifts in an ecologically relevant gene, the chromosomal neighborhood of that gene will also be shifted ( genetic hitchhiking ). This is because recombination cannot effectively shuffle loci in close proximity (linkage) We can therefore use genetic markers to scan the genome for signatures of selection at adaptation genes Hitchhiking with a gene undergoing selective frequency shift Selectively neutral genetic markers Novel, favorable allele at adaptation gene ACGGTGCGC GTAGGCCA ATGGTGCGC GTAGGCAA ATGGTGCGC GTAAGCAA ATGGTGCGC GTAAGCAA ATGGTGCGC GTAAGCAA ACGGTGCGC GTAGGCAA ACGGTGCGC GTAGGCAA ACGGTGCGC GTAAGCAA Chromosome segment Ancestral allele at adaptation gene many generations later Fixation of the novel allele ACGGTGCGC GTAGGCCA ATGGTGCGC GTAGGCCA ACGGTGCGC GTAGGCCA ACGGTGCGC GTAGGCCA ATGGTGCGC GTAGGCCA ACGGTGCGC GTAGGCCA ACGGTGCGC GTAGGCCA ATGGTGCGC GTAGGCCA Genetic hitchhiking 25
25 Genome regions containing a gene under divergent selection between habitats should display exceptionally strong population differentiation max Hitchhiking region Differentiation Genetic marker Candidate gene min Environment A Environment B T T T T T T T T Chromosome G G G G G G G Genetic differentiation is often quantified as F ST (variation among relative to variation within populations) Powerful methods for massive marker generation have recently been developed (see Dieter Ebert s lecture) 26
26 Example: genome scans in marine-freshwater stickleback Freshwater stickleback from four watersheds on Vancouver Island Joe s Misty Robert s Marine (ancestral) stickleback from two coastal sites Marine Boot Genotyping at ~ genome-wide singlenucleotide polymorphisms ( SNPs ) 100 km Calculation of marine-freshwater divergence (F ST ) at every marker Smoothing of the data using sliding window analysis McCairns et al Differentiation along chromosome km Roesti, Salzburger, Berner, in preparation Atp1a1 (N-K exchange) Atp1a1 expression under low and high salinity 27
27 Differentiation along chromosome 4 Ectodysplasin marine freshwater Outlook: high-resolution genome scans in replicate lake and stream stickleback pairs from the Lake Constance basin (Kueng, Moser, Roesti, Berner) F ST Chr7 0.0e e e e e e+07 28
28 Summary Marker-based genome scans, combined with information on gene function, reveal fingerprints of adaptation in the stickleback genome Good replication at the habitat level allows pinning down the ecological context of the genetic shifts High marker resolution and a good reference genome are essential for finding candidate genes (not available in many organisms) Marker data acquisition is rather expensive (still) Approach works only in the early stages of adaptive divergence, where non-selective differentiation between populations is still weak Linking selective signatures to phenotypes might often be very difficult (see QTL mapping, Dieter Ebert s lecture) 29
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