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And Effective Population Size 1/25/2019 Lineage Sorting is a function of time (in Coalescent analyses of genome-scale indel (insertion- generations) and deletion) data provide a unique source of information effective population about avian species tree and ancestral population sizes size (Ne) Edward Braun - University of Florida smaller populations tend to Peter Houde & Nitish Narula - New Mexico State University have more recent common Siavash Mirarab - University of California San Diego ancestors PAG, January 2019 Preview Probability of concordance with species tree For a rooted three-taxon species tree the probability that a gene Background tree matches the species tree is simple: −푡 Indel data 2 2푁e 푃 = 1 − 3 Estimating species trees with indels (Pamilo and Nei 1988 Mol Biol Evol 5:568-583) Avian demography at the K-Pg boundary Where P is the probability that a gene tree matches the species tree, t is the internal branch length (in generations), and Ne is the effective population size Lineage Sorting Hemiplasy Evidence of Hemiplasy and ILS - Time-dependent process - Alleles can have evolutionary by which species lose histories that differ from the ancestral polymorphissm species tree Incongruent gene trees - Result of incomplete lineage through via genetic drift - problem: apparent gene tree incongruence can result sorting (ILS) from incorrect gene phylogenies (will cause the amount ancestral of incongruence to be overestimated) polymorphism ancestral polymorphism the shorter the time Incongruent genetic markers, e.g., transposable elements complete between speciations, - problem: too few and unequally distributed to be free of the more ILS, sampling artifacts complete the more complete hemiplasy Indels improve on these shortcomings because they are a very large data set with limited true homoplasy Robinson et al 2008 PNAS 105:14477-14481 1 1/25/2019 Jarvis et al 2014 Insertion/Deletion (Indel) Data Set1 Available estimates… (from Jarvis et al. 2014) Numbers of Indels ____________________Indel Size Classes_____________________ >1bp >1bp >10bp >100bp <30bp1 Intron Indels 3,918, 322 2,894,642 881,372 75,724 this- study UCE Indels 1,308,980 963,012 333,722 19,745 - Exon Indels - - - - 157,632 Total 5,384,934 3,857,654 1,215,094 95,469 - 1scored from 48 genomes representing all avian orders 2exon indels >30bp were omitted to avoid mis-scoring of transcript variants Indel Frequency and Homoplasy as Function of Length ASTRAL intron tree (nt gene trees) similar and Putative Mutational Origin to Jarvis MP-EST* TENT Medium_ground-finch Zebra_finch American_crow Golden-collared_manakin Indel Rifleman Budgerigar Kea Peregrine_falcon Red-legged_seriema 0.89 Carmine_bee-eater Downy_woodpecker Consistency (%RI = 1.0) = (%RI Consistency Rhinoceros_hornbill Transposable Elements Bar-tailed_trogon Cuckoo-roller Speckled_mousebird White-tailed_eagle Bald_eagle Turkey_vulture Barn_owl Little_egret Dalmatian_pelican Crested_ibis 0.99 Great_cormorant Emperor_penguin Adelie_penguin 0.98 Northern_fulmar Unequal Crossing Over Red-throated_loon 0.54 Sunbittern White-tailed_tropicbird 0.98 0.94 Grey-crowned_crane 0.47 0.46 Killdeer Hoatzin Annas_hummingbird # total indels (log scale) (log indels total # Chimney_swift Replication Slippage Chuck-wills-widow 0.84 MacQueens_bustard Common_cuckoo Red-crested_turaco Brown_mesite 0.8 Yellow-throated_sandgrouse Pigeon 1 2 3 American_flamingo 10 10 10 Great-crested_grebe Chicken Turkey Pekin_duck Common_ostrich indel length (log scale) White-throated_tinamou ASTRAL intron tree (indel gene trees) also Estimating indel species trees similar to Jarvis MP-EST* TENT Medium_ground-finch Zebra_finch American_crow Golden-collared_manakin Rifleman Budgerigar Kea Peregrine_falcon 1. Indel gene trees – generate gene trees using binary Red-legged_seriema 0.98 Carmine_bee-eater Downy_woodpecker 0.97 coded indel data and combine gene trees using a Rhinoceros_hornbill 0.49 Bar-tailed_trogon Cuckoo-roller Speckled_mousebird standard coalescent method (e.g., ASTRAL) White-tailed_eagle Bald_eagle Turkey_vulture Barn_owl 0.97 Crested_ibis Dalmatian_pelican 0.36 Little_egret 2. Direct analysis of indels – treat binary codes for indels Great_cormorant Emperor_penguin Adelie_penguin as bipartitions from gene trees and in the multispecies 0.65 Northern_fulmar Red-throated_loon 0.74 0.51 Sunbittern 0.54 White-tailed_tropicbird coalescent framework Hoatzin 0.8 Grey-crowned_crane 0.63 Killdeer Annas_hummingbird Chimney_swift Chuck-wills-widow 0.47 MacQueens_bustard Common_cuckoo Red-crested_turaco Brown_mesite 0.48 Yellow-throated_sandgrouse 0.99 Pigeon American_flamingo Great-crested_grebe Chicken Turkey Pekin_duck Common_ostrich White-throated_tinamou 2 1/25/2019 ASTRAL UCE tree (nt gene trees) differs… Indel species tree conclusions Medium_ground-finch Zebra_finch American_crow Golden-collared_manakin Rifleman Budgerigar Kea ASTRAL tree generated using UCE nt gene trees 0.85 Peregrine_falcon Red-legged_seriema Speckled_mousebird differs Carmine_bee-eater Downy_woodpecker Rhinoceros_hornbill Bar-tailed_trogon Columbea is not monophyletic Cuckoo-roller 0.96 White-tailed_eagle Bald_eagle Flamingos+grebes sister to all other Neoaves 0.96 Turkey_vulture Barn_owl Little_egret Topology identical to concatenated UCE analyses Dalmatian_pelican 0.62 Crested_ibis Accipitriforms+owl clade sister to Cavitaves Great_cormorant Emperor_penguin Adelie_penguin 0.99 Northern_fulmar Red-throated_loon 0.68 Sunbittern White-tailed_tropicbird ASTRAL tree generated using UCE indel gene even 0.47 Annas_hummingbird 0.79 Chimney_swift Chuck-wills-widow more incongruent (albeit poorly-supported) 0.5 Killdeer 0.98 Hoatzin Grey-crowned_crane Brown_mesite Columbea is not monophyletic 0.78 Yellow-throated_sandgrouse 0.91 Pigeon 0.93 MacQueens_bustard Pigeon sister to all other Neoaves Red-crested_turaco Common_cuckoo Flamingos+grebes sister to “expanded” waterbird clade American_flamingo Great-crested_grebe Chicken Accipitriforms+owl clade sister to most other landbirds Turkey Pekin_duck But seriemas sister to accipitriforms+owls Common_ostrich White-throated_tinamou ASTRAL UCE tree (indel gene trees) differs even more… Direct indel analysis: Quartet scores Medium_ground-finch Zebra_finch American_crow Golden-collared_manakin Rifleman Budgerigar Kea Reflect from the percentage of consistent alleles per tree Peregrine_falcon Carmine_bee-eater Downy_woodpecker branch (in rooted taxon triplets) 0.99 0.97 Rhinoceros_hornbill 0.55 Bar-tailed_trogon Cuckoo-roller Speckled_mousebird White-tailed_eagle Bald_eagle 0.8 Estimated using a novel implementation of ASTRAL for 0.5 Turkey_vulture Barn_owl Red-legged_seriema 1 0.91 Crested_ibis binary data Dalmatian_pelican 0.55 Little_egret Great_cormorant Emperor_penguin Adelie_penguin 0.65 Northern_fulmar Red-throated_loon 100% = complete lineage sorting 0.53 Sunbittern 0.4 White-tailed_tropicbird 0.37 Grey-crowned_crane 33% = random segregation (zero length branch) 0.82 0.41 Killdeer Hoatzin American_flamingo 0.54 Great-crested_grebe Annas_hummingbird Chimney_swift Chuck-wills-widow 1 0.85 MacQueens_bustard see theorem 2 in Sayyari & Mirarab 2016. “Fast Coalescent-Based 0.87 Red-crested_turaco 0.37 Common_cuckoo Brown_mesite Computation of Local Branch Support from Quartet Frequencies.” Yellow-throated_sandgrouse Pigeon Chicken Molecular Biology and Evolution 33 (7): 1654–68 Turkey Pekin_duck Common_ostrich White-throated_tinamou TENT RAxML Phylogram >100bp Indel Quartet Scores Indel species tree conclusions ASTRAL tree generated using intron nt gene trees is similar to Jarvis MP-EST* TENT Division of Neoaves into Columbea and Passerea Accipitriforms+owl clade sister to all other landbirds ASTRAL tree generated using intron indel gene trees also similar to Jarvis MP-EST* TENT Same basal division and positions for accipitriforms + owls 3 1/25/2019 Origin of Neoavian Orders Various N Estimation Analyses Performed e approximately coincident with ASTRAL coalescent quartet scores – calculated from rooted triplets (on which theory of Ne calculation is premised) the K/Pg boundary Using Ancestral State Reconstruction of Generation Lengths • all indels • >1bp indels • >10bp indels • >100bp indels – today’s focus Using Uniform Generation Length • >100bp indels Parsimony %Retention Index (RI)=1.0 – optimized on whole tree • >100bp indels Comparison of Ne Estimates Coalescent >100bp indels Effective Population Sizes through deep time fails to recover 9 clades (due to zero length branches) based on indels1 range = 86,695 to 5,059,926 (same min/max clades all analyses) Coalescent all indels 10,000,000 ) Cretaceous Paleogene e 8,000,000 fails to recover 4 clades N estimates far higher than all other analyses 6,000,000 range = 292,525 to 40,567,438 4,000,000 2,000,000 Parsimony >100bp indels ( Population 0 fails to recover 2 clades 100 95 90 85 80 75 70 65 60 55 50 45 40 35 30 25 20 15 10 5 0 estimates closest to >100bp coalescent Millions of Years Ago range = 39,941 to 9,864,422 1example shown derived from parsimony-scored %RI=1.0 Largest Ne estimates (based on >100bp indels) Ecological Theory of Adaptive Radiation dove/mesite/sandgrouse 5,059,926 parrots/passerines (Psittacopasserae) 2,153,483 Ecological Opportunity bee-eater/woodpecker 1,881,362 (e.g., increased habitat or resources , absence of heterospecific antagonists, relaxation of directional or stabilizing selection) Australaves 1,784,165 crane/shorebird 1,207,281 coly/coural/trogon/hornbill/bee-eater/woodpecker 1,203,717 Ecological Release flamingo/grebe/dove/mesite/sandgrouse
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