Genomic studies of speciation and gene flow

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1 Genomic studies of speciation and gene flow

2 Why study speciation genomics?

3 Why study speciation genomics? Long-standing questions (role of geography/gene flow)

4 Why study speciation genomics? Long-standing questions (role of geography/gene flow) How do genomes diverge?

5 Why study speciation genomics? Long-standing questions (role of geography/gene flow) How do genomes diverge? Find speciation genes

6 Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation 2. Speciation due to selection without isolation evolution.berkeley.edu

7 Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation 2. Speciation due to selection without isolation evolution.berkeley.edu

8 Genomic divergence during speciation 1. Speciation as a bi-product of physical isolation Sd frequency Transect position (km) Cline theory - e.g. Barton and Gale Speciation due to selection without isolation evolution.berkeley.edu

9 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

10 Stage 1 - one or few loci under disruptive selection Gene under selection Genome F ST Feder, Egan and Nosil TiG

11 Stage 2 - Divergence hitchhiking Genome F ST Feder, Egan and Nosil TiG

12 Stage 2b - Inversion Inversion links co-adapted alleles Genome F ST Feder, Egan and Nosil TiG

13 Stage 3 - Genome hitchhiking Genome F ST Feder, Egan and Nosil TiG

14 Stage 4 - Genome wide isolation Genome F ST Feder, Egan and Nosil TiG

15 Some sub-species clearly in stage 1 l Wing pattern races of Heliconius melpomene Heliconius melpomene n b frequency n D frequency position (km) N frequency Yb frequency Transect position (km)

16 Some sub-species clearly in stage 1 l Wing pattern races of Heliconius melpomene B (red/orange patterns) Yb (yellow/white patterns) S. H. Martin et al. Genome Res. 23, (2013). O. Seehausen et al. Nat. Rev. Genet. 15, (2014).

17 Some sub-species clearly in stage 1 l Carrion and hooded Crows F ST Poelstra, J. W. et al. Science 344, (2014).

18 And here is a recent example with multiple islands Malinsky et al., Science 350, 1493 (2015).

19 And here is a recent example with multiple islands Malinsky et al., Science 350, 1493 (2015).

20 And here is a recent example with multiple islands Malinsky et al., Science 350, 1493 (2015).

21 Other species have islands but are they real? Ellegren, et al. Nature 491, 756- (2012).

22 Other species have islands but are they real? Anopheles gambiae and A. coluzzi Formerly M and S forms of A. gambiae Clarkson et al Nature Communications

23 Other species have islands but are they real?

24 Seehausen et al., Nature Reviews Genetics, 2014

25 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

26 Note that sometimes sweeps within species = speciation genes

27 Sweeps across the species barrier can also lead to Fst peaks Double peaks?? Nicolas Bierne, Daniel Berner and others

28 Anopheles M-S divergence Relative divergence higher in low recombination regions - not significant for absolute divergence see also: Charlesworth 1998 MBE Measures of divergence

29

30 No evidence for higher Dxy in wing l Wing pattern races of Heliconius melpomene pattern loci B (red/orange patterns) Yb (yellow/white patterns) S. H. Martin et al. Genome Res. 23, (2013). O. Seehausen et al. Nat. Rev. Genet. 15, (2014).

31 No evidence for higher Dxy in wing l Wing pattern races of Heliconius melpomene pattern loci B (red/orange patterns) Yb (yellow/white patterns) S. H. Martin et al. Genome Res. 23, (2013). O. Seehausen et al. Nat. Rev. Genet. 15, (2014).

32 Suggestion that we use absolute measures of divergence?

33 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

34 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

35 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

36 Explicit tests for gene flow: Neanderthal genome Isolated DNA from bones 38,000 yrs old in Croatia We diverged from Neanderthals around ,000yrs ago Evidence for gene exchange with humans (1-4% of genome?) Green et al., 328:710 Science 2010

37 Explicit tests for gene flow: ABBA- BABA test

38 Explicit tests for gene flow: ABBA- BABA test Green et al Science 328:

39 Explicit tests for gene flow: ABBA- BABA test Gene flow OBSERVE: ABBA BABA

40 Explicit tests for gene flow: ABBA- BABA test Gene flow EXPECT: 50% ABBA 50% BABA OBSERVE: ABBA BABA Green et al Science 328:

41 Explicit tests for gene flow: ABBA- BABA test Gene flow EXPECT: 50% ABBA 50% BABA OBSERVE: ABBA BABA Green et al Science 328:

42 Explicit tests for gene flow: ABBA- BABA test

43 Explicit tests for gene flow: Combining multiple signals

44 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

45 Explicit tests for gene flow: Heliconius butterflies Martin et al., Genome Research 2013

46 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

47 Explicit tests for gene flow: Heliconius butterflies

48 Explicit tests for gene flow: Heliconius butterflies Much larger proportion of genome is flowing as compared to Neanderthals F Similarly strong effect on sex chromosome

49

50

51

52 Sequenced 20 individuals per population at 20x coverage Burri et al., Genome Research 2015

53

54

55 An alternative is to take an explicit modelling approach IM and IMa Jody Hey

56 Martin et al., Biorxiv 2015

57

58

59

60 So far models have mostly just estimated genomewide parameters assuming the genome is homogenous Where we need to go next is to incorporate genome heterogeneity in selection and recombination

61 So far models have mostly just estimated genomewide parameters assuming the genome is homogenous Where we need to go next is to incorporate genome heterogeneity in selection and recombination

62 High density linkage maps to map the recombination landscape Chromosome length (Megabases)

63 The effect of background selection on introgression in humans Harris and Nielson Biorxiv 2015

64 The effect of background selection on introgression in humans Admixture is less in gene rich regions supporting this model.. Harris and Nielson Biorxiv 2015

65 Population and speciation genomics: Conclusions Great power to detect subtle signals of selection and gene flow Can make more general observations about genes and regions involved in adaptation BUT genomic processes complicate the picture Best approaches combine multiple signals to infer process Eventually we need to combine background selection, recombination, positive selection

66 And finally a shameless plug.

67 And finally a shameless plug.

68 Adaptive introgression

69

70

71

72 Photo credit Andrei Sourakov

73 Photo credit Andrei Sourakov

74 Photo credit Andrei Sourakov

75 Photo credit Andrei Sourakov

76

77

78 43 species 77 species

79 Fritz Müller

80 H. melpomene H. cydno F1 hybrid No. Models Attacked Expected number G-test: G = 7.25, d.f. = 1, p = Merrill et al., Proc. Roy. Soc 2012

81

82 Several major loci control Heliconius patterns

83 Several major loci control Heliconius patterns

84 Several major loci control Heliconius patterns

85 Several major loci control Heliconius patterns

86 Several major loci control Heliconius patterns

87 Several major loci control Heliconius patterns

88 Reed et al., 2011 Science

89 E Richard Wallbank

90 Cross-species sharing Heliconius Genome Consortium Nature 2012

91 Cross-species sharing Heliconius Genome Consortium Nature 2012

92 Cross-species sharing Heliconius Genome Consortium Nature 2012

93 Phylogenies across B/D ML tree based on 50,000 bp Heliconius Genome Consortium Nature 2012

94 Phylogenies across B/D ML tree based on 50,000 bp Heliconius Genome Consortium Nature 2012

95 ML tree based on 50,000 bp Phylogenies across B/D

96 ML tree based on 50,000 bp Phylogenies across B/D

97 ML tree based on 50,000 bp Phylogenies across B/D

98 ML tree based on 50,000 bp Phylogenies across B/D

99 ML tree based on 50,000 bp Phylogenies across B/D

100 ML tree based on 50,000 bp Phylogenies across B/D

101 ML tree based on 50,000 bp Phylogenies across B/D

102 ML tree based on 50,000 bp Phylogenies across B/D

103 Okay, so introgression causes mimicry

104 Okay, so introgression causes mimicry But mimicry is weird, right?

105 Novelty can arise through introgression and recombination NNBB Heliconius heurippa Camilo Salazar Mavarez et al., Nature 2006

106 Novelty can arise through introgression and recombination NNBB NNbb Heliconius cydno cordula Heliconius heurippa nnbb Camilo Salazar Mavarez et al., Nature 2006 Heliconius melpomene melpomene

107 Wallbank et al., PLoS Biology kb optix

108 Wallbank et al., PLoS Biology kb optix Red

109 Wallbank et al., PLoS Biology kb optix Blue Red

110 Wallbank et al., PLoS Biology kb optix Blue Red

111 Wallbank et al., PLoS Biology 2016

112 Wallbank et al., PLoS Biology 2016

113 Generate dated trees using this node as a reference point Wallbank et al., PLoS Biology 2016

114 Wallbank et al., PLoS Biology 2016 AB C D E H. numata H. ismenius H. besckei H. nattereri H. ethilla H. hecale H. athis H. luciana H. pardalinus H. elevatus H. melpomene H. timareta H. tristero H. heurippa H. pachinus H. cydno Million Years Ago

115 What about behaviour?

116 What about behaviour?

117 H. melpomene X H. cydno

118 Difference between approaches to cydno and melponmene Number of approaches Richard Merrill bb Bb Genotype

119 Mate preference segregates with forewing colour in backcross hybrids Relative probability of courting H. melpomene females Merrill et al. Proc Roy Soc B, 2011

120 Mate preference segregates with forewing colour in backcross hybrids H. melpomene measured preference Relative probability of courting H. melpomene females Large effect: 35% of the difference between parental species G = 58.64, P << H. cydno measured preference Merrill et al. Proc Roy Soc B, 2011

121 NNbb NNBB Heliconius cydno cordula nnbb Heliconius heurippa Heliconius melpomene melpomene Mavarez et al., Nature 2006

122 Number of approaches cordula heurippa melpomene Melo et al., Evolution 2009

123 Chromosome Now working on QTL maps of species differences in behaviour: LOD score X LOD score X LOD score X

124

125 Lamichhaney et al., Nature 2015

126 Lamichhaney et al., Nature 2015

127 ALX1 associated with beak shape Blunt Pointy

128 Most of these studies use phenotype associations to identify introgressed loci But can we identify them a priori using the ABBA-BABA method?

129 Explicit tests for gene flow: ABBA- BABA test

130 Explicit tests for gene flow: ABBA- BABA test Green et al Science 328:

131 D is quite dependent on the number of informative sites (the denominator) Martin et al., MBE 2014

132 D is not at all good at detecting outlier windows D is quite dependent on the number of informative sites (the denominator) Martin et al., MBE 2014

133 D is not at all good at detecting outlier windows D is quite dependent on the number of informative sites (the denominator) Martin et al., MBE 2014

134 D is not at all good at detecting outlier windows D is quite dependent on the number of informative sites (the denominator) Where s is numerator from the D equation f is the fraction of introgression compared to maximum possible Martin et al., MBE 2014

135 Martin s F Martin et al., MBE 2014

136 But Martin s F is quite good at finding the introgression outliers Martin s F Martin et al., MBE 2014

137 Smith and Kronforst argued that introgression could be inferred where ABBA-BABA outliers showed lower Dxy compared to genome-wide average

138

139

140 Be wary of window based D statistics F is better than D Sampling design is very important!

141 Implications for tree-thinking Archaea Eukarya The tree of life is reticulated Bacteria

142 Implications for tree-thinking Mallet, Hahn and Besansky BioEssays 2015 Hahn and Nakhleh Evolution 2015

143

144 Okay, so what have we learnt and where do we go from here?

Summary. 16 1 Genes and Variation. 16 2 Evolution as Genetic Change. Name Class Date

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