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Investigating the genetic basis of adaptation in a
climate change sensitive species: the American pika
Philippe Henry, November 21st 2011
The Anthropocene
Crutzen, P.J. (2002) Nature
 [CO2 ]
http://www.ipcc.ch/graphics/ar4-wg1/jpg/spm4.jpg
“Unequivocal” warming
http://www.ipcc.ch/graphics/ar4-wg1/jpg/spm5.jpg
Predictions
Biotic responses ?
Move Adapt Disappear
M. Bedart
Biotic responses ?
M. Bedart L. Gooch
Move Adapt Disappear
Biotic responses ?
M. Bedart L. Gooch C. Guthier
Move Adapt Disappear
Disappear = Extinction
Monteverde golden toad
(Bufo periglenes) 1966 - 1989
Pound et al. (1999) Nature; Thomas et al. (2004) Nature; Barnosky et al. (2011)
Nature E. Monk
Move = Range shifts
Upward movement of Alpine
plants
Walther et al. (2005) TREE; Frei et al. (2010) Botanica Helvetica
10 m shift in
elevation per
decade
Move = Range shifts
Pole-ward movement of Animals
Parmesan (1996) Nature, Parmesan & Yohe (2003) Nature B. Bouton
6 km northward
range shift, 6 m
shifts in
elevation per
decade
Move = Range shifts
Fungi are also moving !
Amanita ovoidea is a Mediterranean species now found in the UK C. Gregg
Adapt = Evolution
Réale et al (2003) Proc R Soc B A. De la Cruz
Advanced
breeding time by
18 days per
decade
(6 days per
generations)
The American Pika
Harbinger of climate change
Beever et al. (2003) Journal of Mammalogy; Beever et al. (2011) Global Change Biology;
Smith et al. (2004) Species
R. Howie
The American Pika
Small relative of Rabbits
Specialized Habitat
Talus slopes throughout North
American Mountains
Evidence of susceptibility
Low tolerance to
warm diurnal
temperatures
above 27° C
Mac Arthur & Wang (1974) Canadian Journal
of Zoology
Map with permission from David Hafner
Evidence of susceptibility
30% of populations
have become
extirpated in last
century
Beever et al. (2003) Journal of Mammalogy;
Beever et al. (2011) Global Change Biology;
Map with permission from David Hafner
Evidence of susceptibility
30% of populations
have become
extirpated in last
century
145 m upslope
range retraction in
the last decade
Beever et al. (2003) Journal of Mammalogy;
Beever et al. (2011) Global Change Biology;
Map with permission from David Hafner
Ideal system
Pikas
inhabit
sharp
elevation
gradients
Henry et al. (Submitted)
Northwest Science
Temperature loggers along
elevation gradietn
Average of
7°C difference
from top to
bottom of
transect.
Henry et al. (Submitted)
Northwest Science
Temperature°C
Natural experiment
Three elevation transects
as surrogates for predicted
climate change
Temperature°C
Hair Snares
Henry & Russello (2011) European Journal
of Wildlife Research; Henry et al. (2011)
Journal of Visualized Experiments
Noninvasive sampling
Henry & Russello (2011) European Journal of Wildlife Research;
Henry et al. (2011) Journal of Visualized ExperimentsA. Henry
Hair Samples
168 individuals
15
6
17
26
32
21
10
30
5
6
Lab Work
The Question
Are pikas more likely to
disperse to more favorable
conditions or adapt in situ?
Objectives
1. Assess whether upslope migration
may represent a mitigation strategy to
cope with climate change
2. Investigate the genetic basis of
adaptation. Specifically detect
genomic regions under selection and
identify the environmental drivers
Objectives
1. Assess whether upslope migration
may represent a mitigation strategy to
cope with climate change
2. Investigate the genetic basis of
adaptation. Specifically detecting
genomic regions under selection and
identifying the environmental drivers
10 Microsatellite Loci
Neutral genetic variation (not under selection)
Reflect demographic patterns
Used to investigate population genetic structure and
gene flow
1. Migration across elevations
METHODS
1. Migration across elevations
RESULTS: Isolated populations
Henryetal.(Submitted)PLoSOne
1. Migration across elevations
RESULTS: No Evidence for upslope migration
Henryetal.(Submitted)PLoSOne
Henryetal.(Submitted)PLoSOne
1. Migration across elevations
CONCLUSION
2. Genetic basis of adaptation across
elevation gradients
METHODS
1509 Amplified Fragment Length Polymorphism (AFLP) Loci
Generates a large
number of markers
“Genomic scan”
Doesn’t require
sequence information
Ideal for non-model
organisms
Anonymous
2. Genetic basis of adaptation across
elevation gradients
METHODS
Environmental variables
CLIMATEBC:
Altitude (ALT)
Mean annual temperature
(MAT)
Mean annual precipitation
(MAP)
Precipitation as Snow (PAS)
Summer mean maximum
temperature (Tmax)
Winter mean minimum
temperature (Tmin)
Fst/He
Markers Candidate balancing selection Candidate neutral Candidate positive selection
0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.60
He
-0.1
0.0
0.1
0.2
0.3
0.4
0.5
0.6
Fst
Loci with unusually high divergence  Signature of selection
1.5 % of the genome showed outlier behaviour
2. Genetic basis of adaptation across
elevation gradients
RESULTS
Mean annual precipitation (R2
adj = 0.82, F-test, F=24.6, DF=5, p=0.008)
High frequency of allele at low elevations may confer adaptation to drier conditions
2. Genetic basis of adaptation across
elevation gradients
RESULTS
Low
Mid
High
Summer mean maximum temperature (R2
adj = 0.81, F-test, F=23, DF=5, p=0.009)
High frequency of allele at low elevations may confer adaptation to warmer conditions
2. Genetic basis of adaptation across
elevation gradients
RESULTS
Low
Mid
High
Summer mean maximum temperature (R2
adj = 0.79, F-test, F=20.28, DF=5, p=0.01)
Low frequency at low elevation, may confer adaptation to colder temperatures
2. Genetic basis of adaptation across
elevation gradients
RESULTS
Low
Mid
High
2. Genetic basis of adaptation across
elevation gradients
CONCLUSION
Low
Mid
High
Summary
720 740 760 780 800 820 840
0.40.50.60.70.8
Mean Annual Precipitation (mm)
FrequencyofE38_T32_136
Fst/He
Markers Candidate balancing selection Candidate neutral Candidate positive selection
0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.6
He
-0.100
-0.075
-0.050
-0.025
0.000
0.025
0.050
0.075
0.100
0.125
0.150
0.175
0.200
Fst
PIKA_E31T39_55.6
PIKA_E33T37_107.4
PIKA_E33T37_109.5
PIKA_E43T37_100.6
PIKA_E38T32_85.8
PIKA_E38T37_259.7
PIKA_E44T44_111.4
Upslope migrations will
likely not represent a viable
strategy to cope with
anticipated climate change
20 loci were identified as
under selection and may
thus confer an advantage in
the face of climate change.
MAP and Tmax were
identified as potential
selective forces
Next steps
Isolate and Clone outlier
AFLP fragments
Sanger sequencing of
clones to identify genes
under selection
Next Generation
Sequencing of pika
transcriptome and SNP
discovery
Upslope dispersal will likely not be
a good mitigation strategy
Henryetal.(Submitted)PLoSOne
1. Migration across elevations
RESULTS: No Evidence for upslope migration
Luikart et al. (2003) Nature Reviews
Genetics
Ouborg et al. (2010) Trends in
Genetics
Barret & Hoekstra (2011) Nature
Reviews Genetics
Chevin et al. (2010) PLoS Biology
Chevin et al. (2010) PLoS Biology

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investigating the genetic basis of adapation

  • 1. Investigating the genetic basis of adaptation in a climate change sensitive species: the American pika Philippe Henry, November 21st 2011
  • 6. Biotic responses ? Move Adapt Disappear M. Bedart
  • 7. Biotic responses ? M. Bedart L. Gooch Move Adapt Disappear
  • 8. Biotic responses ? M. Bedart L. Gooch C. Guthier Move Adapt Disappear
  • 9. Disappear = Extinction Monteverde golden toad (Bufo periglenes) 1966 - 1989 Pound et al. (1999) Nature; Thomas et al. (2004) Nature; Barnosky et al. (2011) Nature E. Monk
  • 10. Move = Range shifts Upward movement of Alpine plants Walther et al. (2005) TREE; Frei et al. (2010) Botanica Helvetica 10 m shift in elevation per decade
  • 11. Move = Range shifts Pole-ward movement of Animals Parmesan (1996) Nature, Parmesan & Yohe (2003) Nature B. Bouton 6 km northward range shift, 6 m shifts in elevation per decade
  • 12. Move = Range shifts Fungi are also moving ! Amanita ovoidea is a Mediterranean species now found in the UK C. Gregg
  • 13. Adapt = Evolution Réale et al (2003) Proc R Soc B A. De la Cruz Advanced breeding time by 18 days per decade (6 days per generations)
  • 14. The American Pika Harbinger of climate change Beever et al. (2003) Journal of Mammalogy; Beever et al. (2011) Global Change Biology; Smith et al. (2004) Species R. Howie
  • 15. The American Pika Small relative of Rabbits
  • 16. Specialized Habitat Talus slopes throughout North American Mountains
  • 17. Evidence of susceptibility Low tolerance to warm diurnal temperatures above 27° C Mac Arthur & Wang (1974) Canadian Journal of Zoology Map with permission from David Hafner
  • 18. Evidence of susceptibility 30% of populations have become extirpated in last century Beever et al. (2003) Journal of Mammalogy; Beever et al. (2011) Global Change Biology; Map with permission from David Hafner
  • 19. Evidence of susceptibility 30% of populations have become extirpated in last century 145 m upslope range retraction in the last decade Beever et al. (2003) Journal of Mammalogy; Beever et al. (2011) Global Change Biology; Map with permission from David Hafner
  • 21. Temperature loggers along elevation gradietn Average of 7°C difference from top to bottom of transect. Henry et al. (Submitted) Northwest Science Temperature°C
  • 22. Natural experiment Three elevation transects as surrogates for predicted climate change Temperature°C
  • 23. Hair Snares Henry & Russello (2011) European Journal of Wildlife Research; Henry et al. (2011) Journal of Visualized Experiments
  • 24. Noninvasive sampling Henry & Russello (2011) European Journal of Wildlife Research; Henry et al. (2011) Journal of Visualized ExperimentsA. Henry
  • 28. The Question Are pikas more likely to disperse to more favorable conditions or adapt in situ?
  • 29. Objectives 1. Assess whether upslope migration may represent a mitigation strategy to cope with climate change 2. Investigate the genetic basis of adaptation. Specifically detect genomic regions under selection and identify the environmental drivers
  • 30. Objectives 1. Assess whether upslope migration may represent a mitigation strategy to cope with climate change 2. Investigate the genetic basis of adaptation. Specifically detecting genomic regions under selection and identifying the environmental drivers
  • 31. 10 Microsatellite Loci Neutral genetic variation (not under selection) Reflect demographic patterns Used to investigate population genetic structure and gene flow 1. Migration across elevations METHODS
  • 32. 1. Migration across elevations RESULTS: Isolated populations Henryetal.(Submitted)PLoSOne
  • 33. 1. Migration across elevations RESULTS: No Evidence for upslope migration Henryetal.(Submitted)PLoSOne
  • 35. 2. Genetic basis of adaptation across elevation gradients METHODS 1509 Amplified Fragment Length Polymorphism (AFLP) Loci Generates a large number of markers “Genomic scan” Doesn’t require sequence information Ideal for non-model organisms Anonymous
  • 36. 2. Genetic basis of adaptation across elevation gradients METHODS Environmental variables CLIMATEBC: Altitude (ALT) Mean annual temperature (MAT) Mean annual precipitation (MAP) Precipitation as Snow (PAS) Summer mean maximum temperature (Tmax) Winter mean minimum temperature (Tmin)
  • 37. Fst/He Markers Candidate balancing selection Candidate neutral Candidate positive selection 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.60 He -0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6 Fst Loci with unusually high divergence  Signature of selection 1.5 % of the genome showed outlier behaviour 2. Genetic basis of adaptation across elevation gradients RESULTS
  • 38. Mean annual precipitation (R2 adj = 0.82, F-test, F=24.6, DF=5, p=0.008) High frequency of allele at low elevations may confer adaptation to drier conditions 2. Genetic basis of adaptation across elevation gradients RESULTS Low Mid High
  • 39. Summer mean maximum temperature (R2 adj = 0.81, F-test, F=23, DF=5, p=0.009) High frequency of allele at low elevations may confer adaptation to warmer conditions 2. Genetic basis of adaptation across elevation gradients RESULTS Low Mid High
  • 40. Summer mean maximum temperature (R2 adj = 0.79, F-test, F=20.28, DF=5, p=0.01) Low frequency at low elevation, may confer adaptation to colder temperatures 2. Genetic basis of adaptation across elevation gradients RESULTS Low Mid High
  • 41. 2. Genetic basis of adaptation across elevation gradients CONCLUSION Low Mid High
  • 42. Summary 720 740 760 780 800 820 840 0.40.50.60.70.8 Mean Annual Precipitation (mm) FrequencyofE38_T32_136 Fst/He Markers Candidate balancing selection Candidate neutral Candidate positive selection 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.6 He -0.100 -0.075 -0.050 -0.025 0.000 0.025 0.050 0.075 0.100 0.125 0.150 0.175 0.200 Fst PIKA_E31T39_55.6 PIKA_E33T37_107.4 PIKA_E33T37_109.5 PIKA_E43T37_100.6 PIKA_E38T32_85.8 PIKA_E38T37_259.7 PIKA_E44T44_111.4 Upslope migrations will likely not represent a viable strategy to cope with anticipated climate change 20 loci were identified as under selection and may thus confer an advantage in the face of climate change. MAP and Tmax were identified as potential selective forces
  • 43. Next steps Isolate and Clone outlier AFLP fragments Sanger sequencing of clones to identify genes under selection Next Generation Sequencing of pika transcriptome and SNP discovery
  • 44.
  • 45. Upslope dispersal will likely not be a good mitigation strategy Henryetal.(Submitted)PLoSOne 1. Migration across elevations RESULTS: No Evidence for upslope migration
  • 46. Luikart et al. (2003) Nature Reviews Genetics
  • 47. Ouborg et al. (2010) Trends in Genetics
  • 48. Barret & Hoekstra (2011) Nature Reviews Genetics
  • 49.
  • 50. Chevin et al. (2010) PLoS Biology
  • 51. Chevin et al. (2010) PLoS Biology