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Genomic studies of speciation and gene flow Why study speciation genomics? Long-standing questions (role of geography/gene flow) How do genomes diverge? Find speciation genes Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation 2. Speciation due to selection – without isolation evolution.berkeley.edu Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation 0.8 0.4 frequency d S 0.0 80 100 120 140 160 180 Transect position (km) Cline theory - e.g. Barton and Gale 1993 2. Speciation due to selection – without isolation evolution.berkeley.edu Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation T i m ? e 2. Speciation due to selection – without isolation evolution.berkeley.edu Wu 2001, JEB Stage 1 - one or few loci under disruptive selection Gene under selection Genome FST Feder, Egan and Nosil TiG Stage 2 - Divergence hitchhiking Genome FST Feder, Egan and Nosil TiG Stage 2b - Inversion Inversion links co-adapted alleles Genome FST Feder, Egan and Nosil TiG Stage 3 - Genome hitchhiking Genome FST Feder, Egan and Nosil TiG Stage 4 - Genome wide isolation Genome FST Feder, Egan and Nosil TiG Some sub-species clearly in stage 1 lWing pattern “races” of Heliconius melpomene Heliconius erato Heliconius melpomene 1986 1986 0.8 2011 0.8 2011 n n 1 1 0.4 0.4 frequency 10 frequency 10 b D 50 50 0.0 0.0 80 100 120 140 160 180 80 100 120 140 160 180 0.8 0.8 0.4 0.4 frequency frequency r D C 0.0 0.0 80 100 120 140 160 180 80 100 120 140 160 180 0.8 0.8 0.4 0.4 frequency frequency d N S 0.0 0.0 80 100 120 140 160 180 80 100 120 140 160 180 Transect position (km) 0.8 0.4 frequency b Y 0.0 80 100 120 140 160 180 Transect position (km) Some sub-species clearly in stage 1 lWing pattern “races” of Heliconius melpomene B (red/orange patterns) Yb (yellow/white patterns) S. H. Martin et al. Genome Res. 23, 1817–1828 (2013). O. Seehausen et al. Nat. Rev. Genet. 15, 176–92 (2014). Some sub-species clearly in stage 1 lCarrion and hooded Crows FST Poelstra, J. W. et al. Science 344, 1410–4 (2014). And an example with multiple islands? Malinsky et al., Science 350, 1493 (2015). Other species have islands…but are they real? Ellegren, et al. Nature 491, 756- (2012). Other species have islands…but are they real? Anopheles gambiae and A. coluzzi Formerly M and S forms of A. gambiae Clarkson et al. 2014 Nature Communications Other species have islands…but are they real? Seehausen et al., Nature Reviews Genetics, 2014 What do patterns of Fst really mean? • Fst measures relative divergence • Peaks indicate regions of higher than expected between population divergence, given the within population divergence • Peaks can therefore result from reduced diversity within species • This could be due to lower Ne within species (selective sweeps, background selection) • So peaks NOT NECESSARILY due to reduced gene flow Note that sometimes sweeps within species = speciation genes Sweeps across the species barrier can also lead to Fst peaks Double peaks?? Nicolas Bierne, Daniel Berner and others Anopheles M-S divergence Relative divergence higher in low recombination regions - not significant for absolute divergence see also: Charlesworth 1998 MBE Measures of divergence… More recently see papers by Reto Burri No evidence for higher Dxy in wing pattern loci lWing pattern “races” of Heliconius melpomene B (red/orange patterns) Yb (yellow/white patterns) S. H. Martin et al. Genome Res. 23, 1817–1828 (2013). O. Seehausen et al. Nat. Rev. Genet. 15, 176–92 (2014). Suggestion that we use absolute measures of divergence? Understanding genomic divergence No single statistic will capture the complex history of mutation, migration and selection Patterns need to be interpreted in the specific context of the study species Much better to use explicit tests for gene flow Need to design sampling so the expectations in the absence of gene flow are clear and testable The key is to identify ‘control’ populations that are not influenced by admixture Explicit tests for gene flow: Neanderthal genome •Isolated DNA from bones 38,000 yrs old in Croatia •We diverged from Neanderthals around 270-440,000yrs ago •Evidence for gene exchange with humans (1-4% of genome?) Green et al., 328:710 Science 2010 Explicit tests for gene flow: ABBA- BABA test EXPECT: OBSERVE: 50% ABBA 103612 ABBA Green et al. 2010 Science 328:710-722 50% BABA 94029 BABA Explicit tests for gene flow: ABBA- BABA test Explicit tests for gene flow: ABBA- BABA test Explicit tests for gene flow: Combining multiple signals 1) Derived alleles at high frequency shared with Neanderthal 2) High divergence to Africa but low to Neanderthal 3) Long haplotype blocks The genomic landscape of Neanderthal ancestry in present-day humans - Sankararaman et al. Nature 2014 Sampled 10 complete high coverage genomes per population Explicit tests for gene flow: Heliconius butterflies Many sources of reproductive isolation: Female hybrids are sterile Different host plant use Different habitat preference Strong assortative mating Using Simon Martin’s Twisst method to characterise relationships ABBA-BABA statistics Simon Martin melG melW cyd outgroup Martin et al., MBE 2015 Downloaded from genome.cshlp.org onDownloaded September from 18,Downloaded genome.cshlp.org2013 - Published from genome.cshlp.org by on Cold September Spring Harbor18, on 2013 September Laboratory - Published 18, Press 2013 by Cold - Published Spring Harbor by Cold Laboratory Spring Harbor Press Laboratory Press Downloaded from genome.cshlp.orgDownloaded from ongenome.cshlp.org September 18, Downloaded2013on September - Published from 18, by genome.cshlp.org2013 Cold - PublishedSpring Harbor by on Cold SeptemberLaboratory Spring Harbor18,Press 2013 Laboratory - Published Press by Cold Spring Harbor Laboratory Press 300+ offspring for each cross type John Davey x x x PstI RAD sequencing Linkage maps built (site every ~10kb) with Lep-MAP Davey et al., Evol Letters 2017 617 Figure 2. Four-taxon617 maximum-likelihoodFigure617 2. Four-taxonFigure trees 2. Four-taxon maximum-likelihood for 100 kb maximum-likelihood windows trees for 100 trees kb windowsfor 100 kb windows 618 (A) Trees were superimposed618 (A) using 618Trees Densitree were(A) superimposedTrees (Bouckaert were superimposed using 2010). Densitree There using were (Bouckaert Densitree 2848 trees 2010).(Bouckaert for theThere H. 2010). were There2848 treeswere for2848 the trees H. for the H. 617 Figure617 2. Four-taxonFigure 2. maximum-likelihood Four-taxon617 maximum-likelihoodFigure trees 2. Four-taxonfor 100 treeskb windows maximum-likelihood for 100 kb windows trees for 100 kb windows 619 cydno – H. melpomene619 datasetcydno 619(left) – H. and cydnomelpomene 2453 – forH. melpomenedatasetthe H. timareta(left) dataset and – 2453H. (left) melpomene for and the 2453 H. datasettimareta for the (right). 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    Biological Journal of the Linnean Society, 2007, 92, 221–239. With 4 figures Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data MARGARITA BELTRÁN1,2,3*, CHRIS D. JIGGINS3, ANDREW V. Z. BROWER4, ELDREDGE BERMINGHAM1 and JAMES MALLET2 1Smithsonian Tropical Research Institute, AA 2072, Balboa, Panama 2The Galton Laboratory, Department of Biology, University College London, London NW1 2HE, UK 3Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK 4Department of Biology, Middle Tennessee State University, Murfreesboro, TN 37132, USA Received 22 November 2005; accepted for publication 4 November 2006 Phylogenetic information is useful in understanding the evolutionary history of adaptive traits. Here, we present a well-resolved phylogenetic hypothesis for Heliconius butterflies and related genera. We use this tree to investigate the evolution of three traits, pollen feeding, pupal-mating behaviour and larval gregariousness. Phylogenetic relationships among 60 Heliconiina species (86% of the subtribe) were inferred from partial DNA sequences of the mitochondrial genes cytochrome oxidase I, cytochrome oxidase II and 16S rRNA, and fragments of the nuclear genes elongation factor-1a, apterous, decapentaplegic and wingless (3834 bp in total). The results corroborate previous hypotheses based on sequence data in showing that Heliconius is paraphyletic, with Laparus doris and Neruda falling within the genus, demonstrating a single origin for pollen feeding but with a loss of the trait in Neruda. However, different genes are not congruent in their placement of Neruda; therefore, monophyly of the pollen feeding species cannot be ruled out. There is also a highly supported monophyletic ‘pupal-mating clade’ suggesting that pupal mating behaviour evolved only once in the Heliconiina.