Natural selection and diversification in the threespine stickleback

Delivered at the Duke PopBio Seminar in October 2016.

Transcript

1. Natural selection and diversification in the threespine stickleback Kieran Samuk Postdoc, Noor Lab Department of Biology Duke University Photo: Nicole Bedford
2. Dolph Schluter
3. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
4. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
5. An incipient species of marine threespine stickleback from Nova Scotia, Canada Kieran Samuk* Hannah Visty Dolph Schluter
6. Speciation is the evolution of reproductive isolation (RI)
7. Reproductive isolation takes a wide variety of forms
8. In the absence of geographic isolation, ecologically-mediated barriers are key TROPHIC NICHE IMMIGRANT INVIABILITY POLLINATORS
9. In the absence of geographic isolation, ecologically-mediated barriers are key TROPHIC NICHE IMMIGRANT INVIABILITY POLLINATORS
10. Trophic divergence promotes co-existence and acts an isolating barrier
11. Trophic divergence is a major ecological barrier in a wide variety of animal species
12. Trophic divergence is a major ecological barrier in a wide variety of animal species Freed et al. 1994
13. When animals speciate without geographic isolation, trophic divergence is a key initial barrier …but is it, really? Coyne & Orr 2004, Schluter 2008, Feder et al. 2011
14. When animals speciate without geographic isolation, trophic divergence is a key initial barrier …but is it, really? Coyne & Orr 2004, Schluter 2008, Feder et al. 2011
15. Prediction: very young, sympatric species should differ in trophic niche © Pearson Education 2004
16. Sticklebacks are a key example of speciation via trophic divergence 1 10+ 1 5+ 20+
17. Every described stickleback species pair differs in trophic niche BENTHIC Macroinverts LIMNETIC Copepods LAKE Zooplankton STREAM Macroinverts MARINE Copepods RIVER Macroinverts
18. Most stickleback species pairs are not in the earliest stages of speciation Single population Complete reproductive isolation Lake Stream Benthic Limnetic Japan Sea Pacific Marine
19. Most stickleback species pairs are not in the earliest stages of speciation Single population Complete reproductive isolation Lake Stream Benthic Limnetic Japan Sea Pacific Marine Need to look here!
20. In the absence of geographic isolation, is trophic divergence necessary for speciation in sticklebacks?
21. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in trophic characters
22. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in trophic characters
23. In the 90s, biologists working in Nova Scotia observed odd “white” stickleback Photo: Max Blouw
24. Photo: Max Blouw White and “common” stickleback are sympatric across Nova Scotia
25. Photo: Max Blouw “Common” sticklebacks White and “common” stickleback are sympatric across Nova Scotia
26. Early work found no genetic differences between whites and commons!
27. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in ecological and sexual traits
28. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in ecological and sexual traits ?
30. I sampled white and common stickleback at 12 sites in Nova Scotia
31. I made genotyping-by-sequencing libraries and called variants Demultiplexed reads Trimmomatic BWA + Stampy
32. White and common sticklebacks are genetically distinct
33. The difference is stable across years and includes both males and females White White Common Common
34. Genetic differences between white and commons are found genome-wide FST ≈ 0.01
35. Best fit demographic model is divergence with gene flow ∂a∂i TREEMIX
36. Single population Complete reproductive isolation Lake Stream Benthic Limnetic Japan Sea Pacific Marine
37. Single population Complete reproductive isolation Lake Stream Benthic Limnetic Japan Sea Pacific Marine White Common
38. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in trophic characters
39. Approach • Find stickleback species pair in very early stages of speciation • Test for divergence in trophic characters
41. We measured Carbon-13 and Nitrogen-15 isotopic ratios
42. White and common sticklebacks do not differ in isotopic ratios
43. We measured all stickleback traits with known ecological associations
44. Whites and commons do not differ at “classic” ecologically linked traits Trait Whites are/have… Body shape Not different Dorsal spine length Not different Gill raker number Not different Armor plates Not different Egg weight Not different Body size Smaller Pigmentation Lighter (♂) Testes weight Larger testes (♂)
45. Whites and commons do not differ at “classic” ecologically linked traits Trait Whites are/have… Body shape Not different Dorsal spine length Not different Gill raker number Not different Armor plates Not different Egg weight Not different Body size Smaller Pigmentation Lighter (♂) Testes weight Larger testes (♂)
46. No evidence that white sticklebacks differ in trophic niche
47. Summary • White sticklebacks are the least diverged incipient species of stickleback described to date • No detectable difference in trophic niche
48. In the absence of geographic isolation, is trophic divergence necessary for speciation in sticklebacks?
49. In the absence of geographic isolation, is trophic divergence necessary for speciation in sticklebacks? Not in this case!
50. The earliest stages of speciation do not require trophic divergence Single population Complete reproductive isolation Lake Stream Benthic Limnetic Japan Sea Pacific Marine
51. Is divergence between these two types focused on male sexual traits in general?
52. Divergence in sex-biased genes as a proxy for divergence in sexual traits Leder et al. 2015
53. We found loci that were highly divergent between white and commons
54. Expressed FST outliers tended to be more male-biased in their expression
55. Photo: Max Blouw Speciation via invasion of a novel “sexual niche”?
56. Summary • White sticklebacks are the least diverged incipient species of stickleback described to date • No detectable difference in trophic niche • Male sexual traits seem to be playing a key role in reproductive isolation
57. QUESTIONS?
58. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
59. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
60. Experimental evidence for the role of predation in the evolution of brain size Jan Xue* Kieran Samuk* Diana Rennison
61. The vertebrate brain is physically and functionally compartmentalized
62. Vertebrates differ in the relative size and elaboration of brain structures Northcutt et al. 2002
63. Brain size is strongly positively correlated with body size Wikipedia
64. Relative brain size is correlated with cognitive and sensory performance Kotrschal et al. 2013
65. Brains are thought to be involved in energetic tradeoffs with other tissues Brain Energy Gut Gonads Fat Stores + –
66. There is enormous diversity in brain size within and between species Nieuwenhuys et al. 1998
67. What explains patterns of diversity in brain size?
68. Comparative work suggests that ecology correlates with brain size LIGHT STRUCTURE PREDATION SOCIALITY Moran et al. 2015 Watts 2009 Wikipedia Wikipedia
69. Comparative work suggests that ecology correlates with brain size LIGHT STRUCTURE PREDATION SOCIALITY
70. Many studies suggest that predation favors larger brains in prey species Prey species have larger brains Large-brain fish better survive predation Kotrschal et al. (2013) Kondoh (2010)
71. Hypothesis: Predation favors larger brains
72. Hypothesis: Predation favors larger brains Need controlled, multigenerational selection experiments in naturalistic conditions
73. …Luckily, one of these was already happening! Diana Rennison Seth Rudman
74. The existing experiment took a “variation inflation” approach
76. X 5 F1 hybrid families Benthic Limnetic 1/2 of each family 1/2 of each family POND F2 F3 Measure brains Each family split into two ponds (ten ponds total) F1 TROUT! POND POND F2 F3 POND Measure brains
78. Lab-reared benthics have larger olfactory lobes and telencephla than limnetics OLFACTORY LOBE TELENCEPHALON Larger in benthics Park et al. (2012), Park (2010), Keagy (2014)
79. We dissected brains of experimental fish and measured the lobes Area = πxy OLFACTORY LOBE TELENCEPHALON OPTIC LOBE CEREBELLUM
80. Unexpectedly, predation resulted in a decrease in relative brain size * * *
81. We assessed plasticity by raising offspring of experimental fish in the lab F4 Measure brains TROUT POND CONTROL POND Common environment Offspring of 10 random matings Offspring of 10 random matings
82. Lab-reared offspring of predation fish maintained a smaller optic lobe *
83. Why does predation favor the evolution of smaller brains?
84. Predators force prey into hiding, limiting their interactions with the environment %$@*! PREDATION NO PREDATION Miller et al. 2014
85. The addition of trout also causes a variety of other ecological changes Lower phytoplankton biomass Lower zooplankton biomass Greater abundance of large zooplankton Rudman et al. 2016
86. We are working on assessing if brain size is independent from other traits Correlated selection QTL Brain Size
87. Also working on finer characterizations of brain size differences using micro-CT
88. Summary • Contrary to previous results, predation selected for smaller-brained individuals • How predation affects brain evolution is likely highly context dependent – bigger not always better! • Selection experiments are a viable method for exploring the evolutionary ecology of the vertebrate brain
89. QUESTIONS?
90. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
91. SPECIATION & ECOLOGY BRAIN EVOLUTION ADAPTATION GENOMICS
92. Natural selection and gene flow shape the genomic architecture of adaptation in threespine stickleback Kieran Samuk* Greg Owens Sara Miller Kira Delmore Diana Rennison Dolph Schluter
94. Hundreds of studies have found signatures of selection in the genome
95. We know that signatures of selection are ubiquitous in the genome Seehausen et al. Nat Rev. Gen. 2014
96. Why do we see adaptation in some regions of the genome and not others? ? ? Seehausen et al. Nat Rev. Gen. 2014
97. Are there general constraints on where adaptation can occur in the genome? …or can it happen anywhere that adaptive variation is available?
98. Recent theory suggests that gene flow can constrain where adaptation occurs in the genome. Bürger & Akerman 2011 (Theor Popul Biol) Yeaman & Whitlock 2011 (Evolution)
99. Scenario: divergent selection in two populations with a shared ancestor
100. Selection builds up sets of co-selected alleles
101. Gene flow + recombination breaks apart sets of co-selected alleles
102. Tight linkage can prevent allele sets from being broken apart
103. Tight linkage can prevent allele sets from being broken apart
104. Maintained! Broken! Tight linkage can prevent allele sets from being broken apart
105. Highest fitness Tight linkage can prevent allele sets from being broken apart
106. Goal: Test this prediction! Divergent selection + gene flow favors tightly linked clusters of locally-adapted alleles Bürger & Akerman 2011 (Theor Popul Biol) Yeaman & Whitlock 2011 (Evolution)
107. Goal: Test this prediction! Divergent selection + gene flow favors tightly linked clusters of locally-adapted alleles Bürger & Akerman 2011 (Theor Popul Biol) Yeaman & Whitlock 2011 (Evolution)
108. “DS-GF” = Divergent selection with gene flow
109. Problem: Other processes cause “clustered” signatures of selection
110. Gene density and mutation rate variation also cause clustering
111. Hitchhiking causes “clustered” signatures of selection
112. Statistical controls Compare DS+GF to selection and gene flow alone There are solutions to both these issues:
113. Approach • Classify pairs of populations based on presence of selection and/or gene flow • Find loci that are adaptively differentiated between each pair of populations • Quantify the degree of clustering of adaptive loci in the genome, controlling for mutation + gene density
114. Sticklebacks are an excellent system for applying this approach!
116. Approach • Classify pairs of populations based on presence of selection and/or gene flow • Find loci that are adaptively differentiated between each pair of populations • Quantify the degree of clustering of adaptive loci in the genome, controlling for mutation + gene density
117. Parallel Selection Divergent Selection Gene flow Allopatry Idea: compare clustering among different selection and gene flow regimes
118. We used morphological differences as a proxy for divergent selection Divergent Parallel Benthic vs. Limnetic Alaska Marine vs. Oregon Marine
119. We used geographic distance + barriers as a proxy for gene flow 1. No physical barriers 2. < 500 km apart All pairs of stickleback populations with evidence of recent gene flow
120. Approach • Classify pairs of populations based on presence of selection and/or gene flow • Find loci that are adaptively differentiated between each pair of populations • Quantify the degree of clustering of adaptive loci in the genome, controlling for mutation + gene density
121. We found signatures of selection using FST outliers between pairs of populations
122. FST outliers = enriched for adaptive loci
123. Parallel Selection Divergent Selection Gene flow Allopatry We performed FST scans for selection for population pairs in each category
124. Example: one chromosome in one pair of populations per regime
125. Example: one chromosome in one pair of populations per regime
126. Approach • Classify pairs of populations based on presence of selection and/or gene flow • Find loci that are adaptively differentiated between each pair of populations • Quantify the degree of clustering of adaptive loci in the genome, controlling for mutation + gene density
127. DS+GF favors tightly linked clusters of locally-adapted alleles Bürger & Akerman 2011 (Theor Popul Biol) Yeaman & Whitlock 2011 (Evolution)
128. We measured “nearest neighbor” genetic distances between all SNPs vs. outliers All SNPs Outliers only
129. Outliers from DS-GF comparisons were unusually close together in the genome
130. Outliers from DS-GF comparisons were unusually close together in the genome DS+GF
131. Outliers from DS-GF comparisons were unusually close together in the genome *** Permutation test p = 0.0015
132. As predicted, adaptive alleles are more tightly linked in DS-GF comparisons
133. As predicted, adaptive alleles are more tightly linked in DS-GF comparisons What does this actually look like in the genome?
135. Recombination rate
136. Low recombination
137. We quantified the tendency for outliers to occur in regions of low recombination
138. We quantified the tendency for outliers to occur in regions of low recombination
139. We quantified the tendency for outliers to occur in regions of low recombination
140. We quantified the tendency for outliers to occur in regions of low recombination
141. Outliers occurred more often in regions of low recombination in DS-GF pairs Outlier Recombination Bias More biased toward Low recombination Less biased toward Low recombination
142. DS+GF favors tightly linked clusters of locally-adapted alleles
143. DS+GF favors tightly linked clusters of locally-adapted alleles …via concentration of these alleles in regions of low recombination
144. Bürger & Akerman 2011 (Theor Popul Biol) Yeaman & Whitlock 2011 (Evolution)
145. Implications
146. Gene flow may make the usable area of the genome effectively “smaller”
147. Gene flow may make the usable area of the genome effectively “smaller”
148. Smaller set of genes = More re-use of same genes DS+GF = more parallelism? Less variation available overall Novel effect of gene flow?
149. Summary • Gene flow favors the clustering of adaptive alleles in regions of low recombination • May be an important and general constraint on adaptive evolution
150. THANKS!
151. Acknowledgements Kate Ostevik Marius Roesti Sam Yeaman Armando Geraldes Mark Ravinets Anne-Laure Ferchaud Jun Kitano Thor Veen Seth Rudman Baocheng Guo Semiahmoo First Nation Waycobah First Nation Funding Committee Dolph Schluter Mike Whitlock Trish Schulte Loren Rieseberg
152. Heterozygosity vs. recombination does not vary among regimes
153. DS+GF remains more clustered when we control for genome-wide FST
154. Results are qualitatively similar when we use continuous distance
155. Dxy trends in the same direction, but difference is not significant