Separating Population Structure from Recent Evolutionary History
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1 Separating Population Structure from Recent Evolutionary History
2 Problem: Spatial Patterns Inferred Earlier Represent An Equilibrium Between Recurrent Evolutionary Forces Such as Gene Flow and Drift. E.g., f st 1 4N ev µ+1 But, Can Obtain The Same Pattern Due to Recent Historical Events That Have Not Had Time to Reach Equilibrium
3 To Examine Historical Events & Non-Equilibrium States, Need to Study Genetic Variation in Both Space & Time Directly Sample Populations From the Past Reconstruct Variation Through Time Indirectly
4 Sampling/Data depend on question
5 Direct Study: Ancient DNA Neandertals extinct 30,000 YA, but overlapped with modern humans Did they interbreed? Neandertal DNA from 4 sites in Eurasia Compared with modern human DNA from Africa, Europe, and Asia Green et al 2010
6 Neanderthals have more differences from Africans than from non-africans = GENE FLOW
7 Indirect Studies After just 1 generation of random mating get HW frequencies But, when consider >1 site, linkage disequilibrium can persist for a long time [remember D t =D 0 (1-r) t ] Therefore, multi-locus or multi-site polymorphic data can be used to reconstruct history (e.g. admixture)
8 Multiple Loci: Principle Component Analysis of Genetic Data Linkage Disequilibrium is calculated for only 2 loci at a time For many sites, this becomes unwieldy Principal Component Analysis (PCA) often used to examine multivariate data First axis aligned to capture the maximum amount of variation in this multivariate spaces Second axis is orthogonal the the 1 st such that it captures the maximum remaining variation And so on: # of dimensions increases with the # of variables
9 If multilocus associations among demes, then most of the variation in how populations differ genetically will be in the 1 st principal component
10 Multiple Loci: Principle Component Analysis of Genetic Data This procedure has long been used in human genetics to extract multi-locus information about gene flow patterns (e.g., Cavalli-Sforza & Ammerman, 1984). 1 st Principal Component plotted on map for 95 allele frequencies #s = a ranking of the values of the 1 st principal component Same pattern observed in the archeological record for the spread of agriculture out of the Middle East: genetic cline resulted from agriculturalists spreading North
11 Multiple Loci: Principle Component Analysis of Genetic Data Novembre et al. Nature 31 Aug Based on 197,146 loci in 1,387 individuals.
12 Haplotypes=genetic state of many polymorphic sites within a DNA region, often low/no recombination When new haplotype arises, it s restricted geographically = globally rare, tip haplotype Coalescent Theory implies such haplotypes are recent, are not in equilibrium, and have limited spatial distributions Therefore, Globally Rare, Tip Haplotypes Provide A Straightforward Method of Observing The Movements of Genes Through Space Over Short and Recent Time Periods.
13 Geographic distribution of the Asian and American populations genotyped for the microsatellite D9S1120 Schroeder, K. B. et al. Mol Biol Evol : Private 9-repeat allele
14 Haplotype Trees Can examine the spatial/temporal pattern of genetic variation, while F statistics only apply to current spatial pattern Are biologically meaningful only when recombination is absent or rare Gives some information about temporal ordering of Mutational Variation, both the rare and the common mutations Not limited to recent events, but can go back further in time (but not beyond the most recent common ancestral DNA molecule)
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16 It is dangerous to equate a haplotype tree to a species tree. It is NEVER justified to equate a haplotype tree to a tree of populations within a species because the problem of lineage sorting is greater and the time between events is shorter. Moreover, a population tree need not exist at all.
17
18 Nested Clade Analysis Converts Haplotype Trees Into A Nested Statistical Design Other Data (Phenotypic or Geographical) Are Then Overlaid Upon The Nested Design Statistical Tests Are Performed To Detect Significant Associations Between the Data and The Haplotype Tree DOES NOT EQUATE THE HAPLOTYPE TREE TO A POPULATION TREE! Uses only close relationships within tree and not overall tree topology.
19 Can get temporal information from a haplotype tree without a molecular clock Use tree to define a series of hierarchically nested clades (branches within branches) Temporal information because the age of a specific haplotype must be < or equal to the age of the clade it is nested in (nesting clade) If the tree is rooted, get a set of nested hierarchies where every clade is younger than the clade it is nested in
20 A Haplotype Tree In Elephants
21 Nested Clades: Geographical information from sampling Clade Distance D c measures how widespread the clade/haplotype is, weighted by local clade frequencies Nested Clade Distance D n = the avg distance that an individual with a haplotype from a clade/haplotype lies from the geographical center of the nesting clade
22 A Haplotype Tree In Elephants Amboseli Tsavo Hwange Matetsi Sengwa Victoria Falls
23 Isolation by Distance Clade distances should increase over time Older clades should be more widespread than younger clades New/young haplotypes should be within the geographic range of its most recent haplotype ancestor
24 Only When Statistical Significance Is Achieved Is The Biological Significance Interpreted With Explicit, a priori Criteria Within 1-Step Clades Within Total Tree Haplotypes No. in sample D c D n 1-Step Clades D c D n Old haplotypes have larger clade distances than younger haplotypes : Expected with IBD L*** 1027 L*** S*** 657 S*** L*** Old-Young 944 L*** 373 L*** L*** 832 L*** S* S* S*** 768 S*** Old-Young 862 L*** 598 L*** S*** 759 S** Old-Young L*** 409 L***
25 A Haplotype Tree In Elephants Amboseli Tsavo Hwange Matetsi Sengwa Victoria Falls Gene flow with IBD Gene flow with IBD Gene flow with IBD Gene flow with IBD
26 Historical Events Leave Lasting Patterns in Haplotype Trees. Present Area A Area B Area C Range expansion: haplotypes in populations that expanded will become widespread (large D c ) Past Black allele and descendants become widespread, even though other alleles in the original population
27
28 Historical Events Leave Lasting Patterns in Haplotype Trees: Population Fragmentation Haplotypes that arise after an isolation event cannot spread Over time, mutations accumulate which result in larger than average branch lengths between clades in different isolates
29 Fragmentation Inferences From NCA All 5 DNA regions had a different topology with respect to the 3 elephant taxa (only BGN gave a clean fragmentation ); yet NCPA inferred a fragmentation event between forest and savanna elephants in all 5 DNA regions. BGN Y-DNA mtdna Past Fragmentation Followed By Range Expansion and Secondary Contact PLP Past Fragmentation PHKA2
30 Nested Clade Phylogeographic Analysis Recurrent Gene Flow, Range Expansion and Fragmentation Could All Have Occurred at Different Times and/or Places. NCPA Therefore Looks For Multiple Patterns, Not Just One The Relative Temporal Ordering of Events in a Nested Series of Clades Is Also Inferred by NCPA
31 Range Expansion Secondary Contact Isolation by Distance Fragmentation Isolation by Distance Inferences from mtdna haplotype tree of Ambystoma tigrinum from NCPA and supplemental test for secondary contact (Mol. Ecol. 10: , 2001)
32 By Analyzing Haplotype Trees for mtdna, Y- DNA, X-linked DNA and Autosomal DNA, One Can Sample A Wide Variety of Time Scales and Both Male and Female Mediated Gene Flow and Historical Events By Analyzing Multiple Haplotype Trees Can Statistically Correct For The Evolutionary Stochasticity of The Coalescent Process For Any One Genomic Region
33 Inference Errors in Nested Clade Analysis Inference Requires That An Appropriate Mutation Occurred At the Right Time and Right Place: Therefore, Some Events and Processes Are Missed With A Particular DNA Region. Selection and Evolutionary Stochasticity Can Distort The Distribution of Haplotypes in Space and Time, Thereby Leading to False Positive Inferences. These errors can be minimized by studying multiple loci and requiring each inference (type, place and time) to be crossvalidated by two or more loci.
34 Estimated Times To Common Ancestor (Method of Takahata et al. 2001) D hc Nuc.Diff. Between Humans & Chimps D h Nuc.Diff. Within Humans TMRCA = 12D h /D hc 6 Million Years Ago
35 A Likelihood Ratio Test of The Hypothesis That The Estimated Times of An Event From j Loci Are The Same
36 Fragmentation Inferences From NCA Null Hypothesis: there was a single fragmentation event between forest and savanna elephants. Y-DNA mtdna log-likelihood ratio test = with 4 degrees of freedom, p= Accept Null Hypothesis, with T = 4.2 MYA. There are at least 2 lineages of African Elephants. BGN Past Fragmentation Followed By Range Expansion and Secondary Contact PLP Highly Significant Fragmentation Events Found In All Five Haplotype Trees Past Fragmentation PHKA2
37 Performed Nested Clade Analyses on 25 DNA Regions in Humans Mitochondrial DNA (Ingman et al. Nature 408, , 2000: Sykes et al. American Journal of Human Genetics 57, , 1995; Torroni et al. American Journal of Human Genetics 53, , 1993, American Journal of Human Genetics 53, , 1993). Y-DNA (Hammer et al. Molecular Biology and Evolution 15, , 1998) 11 X-Linked Regions (Balciuniene et al. 2001; Garrigan et al. 2005; Hammer et al. 2004; Harris. & Hey, 1999, 2001; Kaessmann et al. 1999; Nachman et al. 2004; Saunders et al. 2002; Verrelli et al. 2002; Yu et al. 2002) 12 Autosomal Genes (Bamshad et al. 2002, Harding et al. 1997; Hollox et al. 2001; Jin et al. 1999; Koda et al. 2001; Rana et al. 1999; Rogers et al. 2000; Toomajian and Kreitman 2002; Wooding et al. 2002; Zhang & Rosenberg 2000).
38 P = 0.95 Three Out-of-Africa Events, All Defined By Three or More Loci With A High Degree of Temporal Homogeneity P = 0.51 But With Highly Significant Heterogeneity Between The Three Events P = 0.62 The log likelihood ratio test rejects the null hypothesis that all 15 events are temporally concordant with a probability value of
39 Inferences of Gene Flow That Are Concordant Geographically Are NOT Necessarily Concordant Temporally Because Gene Flow is a Recurrent Process. However, We Can Test The Null Hypothesis of NO GENE FLOW Between Two Geographical Regions Over a Specified Time Interval.
40 Gamma Distributions For 19 African/ Eurasian Gene Flow Inferences With Isolation By Distance Extensive overlap implies cross-validation with the exception of MX1, the only locus with most of its probability mass in the Pliocene. The lack of clusters implies there was no prolonged breaks in gene flow throughout the Pleistocene
41 Testing The Null Hypothesis of No African/Eurasian Gene Flow Throughout the Pleistocene The Null hypothesis of isolation (no gene flow) in this time interval is rejected with p < 10-8
42 Approaches to phylogeographic analysis exploratory: minimally parameterized methods that are usually concerned with one simple component of evolutionary history NCPA considers evidence for several different components (past vicariance, expansion etc ) model-driven: methods that employ highly parameterized models to represent fullydefined population divergence scenarios
43 Garrick et al 2010
44 Coalescent Simulations Set of Fully Specified Phylogeographic Hypotheses Simulate Coal. Process Many Times Under Each Hypothesis Virtual Current Generation Real Current Generation Draw Simulated Sample of Same Size as Real Sample Statistics on Simulated Sample Statistics from Real Sample Compare Relative Fits of The Simulated Statistics Under Each Model to The Observed Statistics
45 Interpretive Criteria Simulations assign probabilities to complex models as a whole, making it impossible to interpret the biological reason for a low probability. In contrast, NCPA allows individual components to be tested, making the biological interpretation clear.
46 Interpretive Criteria Although Fagundes et al. (2007) interpreted the rejection of their assimilation model as a rejection of admixture, the confounded nature of simulation inference means that such an interpretation has no logical validity. NCPA allows individual components to be tested, making it clear that the part of their assimilation model that is wrong is NOT admixture, but rather the assumption of prior isolation of archaic Africans and Eurasians. X
47 Statistical Phylogeography NCPA and simulation approaches are not so much alternative techniques as they are complementary, and potentially synergistic, techniques. Both add to the statistical toolkit of intraspecific phylogeographers, and both should be used when appropriate.
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