Tenure talk at SBU Fall 2013

1. When models mislead
Liliana M. Dávalos
Assistant Professor, Department of Ecology & Evolution
SUNY, Stony Brook
SUNY Stony Brook
25 September 2013

2. My lab’s research mission
Biological
diversity
Diversificatio
n
Human
impact

3. Two kinds of questions
Biological
diversity
Diversificatio
n, increase decrease Habitat loss

4. The limits of models
• In phylogenetics
• Models missing key biology
• Improving phylogenetic models
• How phenotypes evolve
!
• In environmental change
• Drivers of forest loss

5. The limits of models
• In phylogenetics
• Models missing key biology
• Improving phylogenetic models
• How phenotypes evolve
!
• In environmental change
• Drivers of forest loss

6. Phylogenetics
Mycobacterium bovis BCG str. Pasteur 1173P2
M. tuberculosis H37Ra
M. bovis BCG str. Tokyo 172
M. bovis AF212297
M. tuberculosis CDC1551
pathogenic M. tuberculosis F11
(avium-M. tuberculosis KZN 1435
M. tuberculosis H37Rv
non-pathogenic Mycobacterium smegmatis M. avium subsp. paratuberculosis K10
M. avium 104
M. vanbaalenii PYR1
M. sp. Spyr1
M. smegmatis str. MC2 155
M. sp. KMS
M. sp. MCS
M. sp JLS
Mycobacterium sp. *
Nocardia farcinica IFM 10152
Gordonia bronchialis DSM 43247
Rhodococcus opacus B4
R. equi ATCC 33707
R. equi 103S
Segniliparus rotundus DSM 44985
Bifidobacterium longum NCC2705
B. longum DJO10A
B. longum subsp. infantis 157F
B. longum subsp. longum JCM 1217
B. longum subsp. longum BBMN68
B. longum subsp. infantis ATCC 55813
B. longum subsp. longum JDM301
B. longum subsp. infantis ATCC 15697
B. breve DSM 20213
B. dentium Bd1
B. dentium ATCC B. adolescentis ATCC B. bifidum PRL2010
100
100
84
96
42
100
63
63
65
55
51
70
84
74 100
98
92
99
74
100
100
100
75
99
100
20
88
• All of comparative
biology
• Historical
biogeography
• Evolutionary aspects
of community ecology
• Diagnostics and
similar applications
Corthals...Dávalos 2012 PLoS One
Models missing key bio

7. Phylogenetics
Mycobacterium bovis BCG str. Pasteur 1173P2
M. tuberculosis H37Ra
M. bovis BCG str. Tokyo 172
M. bovis AF212297
M. tuberculosis CDC1551
pathogenic M. tuberculosis F11
(avium-M. tuberculosis KZN 1435
M. tuberculosis H37Rv
non-pathogenic Mycobacterium smegmatis M. avium subsp. paratuberculosis K10
M. avium 104
M. vanbaalenii PYR1
M. sp. Spyr1
M. smegmatis str. MC2 155
M. sp. KMS
M. sp. MCS
M. sp JLS
Mycobacterium sp. *
Nocardia farcinica IFM 10152
Gordonia bronchialis DSM 43247
Rhodococcus opacus B4
R. equi ATCC 33707
R. equi 103S
Segniliparus rotundus DSM 44985
Bifidobacterium longum NCC2705
B. longum DJO10A
B. longum subsp. infantis 157F
B. longum subsp. longum JCM 1217
B. longum subsp. longum BBMN68
B. longum subsp. infantis ATCC 55813
B. longum subsp. longum JDM301
B. longum subsp. infantis ATCC 15697
B. breve DSM 20213
B. dentium Bd1
B. dentium ATCC B. adolescentis ATCC B. bifidum PRL2010
100
100
84
96
42
100
63
63
65
55
51
70
84
74 100
98
92
99
74
100
100
100
75
99
100
20
88
• Diagnostics and
similar applications
• Phylogenetics enables
testing relatedness
Models missing key bio
Corthals...Dávalos 2012 PLoS One

8. Dated trees more
important than ever
• (We need fossils)
• Testing models of trait
evolution
• Understanding history
of assemblages in time
and space
• Testing key
innovations
Dumont, Dávalos et al. 2012 P R Soc B
Models missing key bio

9. Questions
• How good are existing
models for
morphology?
• Characteristics of
the data
• Compare to models
molecular evolution
Dávalos & Russell 2012 Ecol Evol
Models missing key bio

10. Species Characters
What do I mean by
morphological characters?
• They look like this —>
• Discontinuous
between species
• Factors, not
numbers
• Difficult to model
Models missing key bio

11. The organisms in
question Phyllostomidae and relatives
Models missing key bio

12. p
i
i
p p
p
p p D
D
p
p D
pi
D p D
i
p p D
p D
p D
i
i p D
p D
p
p D i
pi
i Di
DD
D
D Di
pi
p D
p p D
p D
Di
p D i D
p D i D
p D D

13. p
Di
D D
D i
D i
D i i
Dp i
p
p
p p
p i
D p
p
D
Di
p D
p
p
D
D i
•
•
Ma
r M
r M aM
r M Ma
r M aM
rM M
r
a
a
ra
M Ma
ra
M
M
r
r M a
r
r r
ra
M r M
a
r r M
a
a r M
r M
r
r M
r M
r r M c
r r M rc M

14. r
Ma
r
r
r
r
Mr a
r
M
M r
M a
a
M a
M
Ma
r
M
r M

15. •
Baker et al. 2003 Occas Pap Mus TTU
Dávalos, Cirranello et al. 2012 Biol Rev
Wetterer et al. 2000 B Am Mus Nat Hist
Models missing key bio

16. The trouble with
morphological characters
• At first, only model
was parsimony
• Neutral Jukes-Cantor
1969 model
implemented 2001
• Applying this model
does not solve conflict
Dávalos, Cirranello et al. 2012 Biol Rev
Models missing key bio

17. If the Jukes-Cantor model is not enough, then
what else could be going on?

18. Non
consistent
q
p
p p
q
Homoplasy I: inconsistency!
Felsenstein 1978 Syst Biol
Models missing key bio
consistent

19. Homoplasy II:
convergent adaptation
• Can bring together
unrelated ecologically
similar lineages
• This example: mt
c
cytochrome b gene
of nectar-feeding
bats
• Association adaptive
molecular evolution
and supporting wrong
node Dávalos, Cirranello et al. 2012 Biol Rev
P e

20. c
P r e e
c

21. A B
e

22. Models missing key bio

23. Homoplasy III:
correlated evolution
• Expected in protein-coding
genes
• Models in use for
codons, aminoacids,
ribosomal RNA
secondary structure
Dávalos Perkins 2008 Genomics
Models missing key bio

24. Might these affect morphological characters?
Reviewer 1:
I don't see the point. If the characters are good
characters (meaning that they have some phylogenetic
signal at some level), then there is nothing especially
wrong with the fact that they are weighted a little more
than other characters.
Models missing key bio

25. Dávalos, Cirranello et al. 2012 Biol Rev
Inconsistency!
Models missing key bio

26. ●
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27. ï
RUQHFWDUï

28. ●
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c
A
e
r P P P

29. Dávalos, Cirranello et al. 2012 Biol Rev
Dávalos et al. Accepted Syst Biol
Convergent
evolution!
Models missing key bio

30. Dávalos et al. Accepted Syst Biol
Correlated evolution!
Dissimilarity between characters -
Models missing key bio

31. Models missing key
biology
• Morphology =
phenotype
• Neutrality and
independence wrong
assumptions
• Not neutral
• Not independent
Skelly et al. 2013 Genome Res
Models missing key bio

32. Morphology
...
Aminoacids
Codons
Why we aren’t there yet
Neutral
genotype
Model complexity
Models missing key bio

33. The limits of models
• In phylogenetics
• Models missing key biology
• Improving phylogenetic models
• How phenotypes evolve
!
• In environmental change
• Drivers of forest loss

34. Analytical innovations
• Statistical scaffolds
• Condition
morphological
resolution on
molecular posterior
• Morphological
simulations
• Uncover significantly
conflicting
characters
Dávalos et al. Accepted Syst Biol
Photos: M. Tschaptka E. Kalko

35. The limits of models
• In phylogenetics
• Models missing key biology
• Improving phylogenetic models
• How phenotypes evolve
!
• In environmental change
• Drivers of forest loss

36. How does
morphology evolve?
• Ordering: each
character state gives
rise to a finite range of
states
• Evidence of limits to
states driven by
• Development
• Natural selection
Dávalos, Cirranello et al. 2012 Biol Rev
How phenotypes evolve

37. Modeling selection in
morphology
• Brownian motion vs.
Ornstein-Uhlenbeck
models
• Continuous
phenotypic traits
• Might selection for
performance explain
homoplasy in
morphological data?
How phenotypes evolve
Butler King 2004 Am Nat

38. OU2b
OU3
nectarivorous
nectarivorous
strictly frugivorous (figs, Short-faced bats)
A B C D
OU2a
nectarivorous
other
frugivorous (figs)
other
frugivorous (figs)
other
frugivorous (figs)
other
OU4
Macrotus
Desmodus
Diaemus
Diphylla
Micronycteris
Lampronycteris
Carollia
Sturnira
Mesophylla
Vampyressa
Platyrrhinus
Vampyrodes
Chiroderma
Metavampyressa
Uroderma
Ardops
Ariteus
Figure Stenoderma
Ametrida
Centurio
Pygoderma
Sphaeronycteris
Artibeus
Ectophylla
Enchisthenes
Rhinophylla
Lonchophylla
LPolantcahlinoaphylla
Choeroniscus
Choeronycteris
Hylonycteris
Anoura
Glossophaga
Leptonycteris
Monophyllus
Erophylla
Phyllonycteris
Brachyphylla
Chrotopterus
Vampyrum
Lophostoma
Phyllostomus
Phylloderma
Mimon
Tonatia
Trachops
Dumont ... Dávalos In Review Evolution
Engineering model of
performance
How phenotypes evolve

39. 500
400
300
200
100
0
0.0 0.4 0.8 1.2
MA
count
diet
figs
figs only
nectar
other
Three performance
peaks
• Performance related to
diet
• Low MA in nectar-feeding
bats
• Convergence on
this phenotype
• Analyzing function and
integrating selection
better than ignoring
Dumont ... Dávalos In Review Evolution
How phenotypes evolve
Mechanical advantage
Frequency

40. Function just as
important in genome
• What drives diversity of
olfactory receptors (OR)?
• OR largest gene family
in mammals
• Prior: variation ~ sensory
modes
• Echolocation
• Development of
vomeronasal organ
• Alternative: Feeding
ecology
Hayden, Dávalos et al. In Review Mol Biol Evol
How phenotypes evolve
OR subfamily
Species

41. Diet ● ●
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Eumops auripendulus ●
Myotis lucifugus
Trachops cirrhosus
Lophostoma silvicola
Vampyrum spectrum
Phyllonycteris poeyi
Erophylla bombifrons
Leptonycteris curasoae
Anoura geoffroyi
Vampyrodes caraccioli
Platyrrhinus helleri
Artibeus jamaicensis
Sturnira tildae
Carollia perspicillata
Desmodus rotundus
Macrotus californicus
Pteronotus parnellii
Thyroptera tricolor
Emballonura atrata
Rhinolophus hipposideros
R. ferrumequinum
Craseonycteris thonglongyai
Nyctimene albiventer
Cynopterus sphinx
Pteropus rayneri
P. giganteus
Rousettus lanatus
●
● ●
●
● ●
●
Animalivorous
Plant-visiting
Fruit specialist
Echolocation
No echolocation
Has VNO
No VNO
Eau
Mlu
Tci
Lsi
Vsp
Ppo
Ebo
Lcu
Age
Vca
Phe
Aja
Sti
Cpe
Dro
Mca
Ppa
Ttr
Eat
Rhi
Rfe
Cth
Nal
Csp
Pra
Pgi
Rla
:
Not sensory system,
but diet
• Only NW frugivores
highly differentiated
• Enriched for OR1/3/7
• Lose OR 5/8/9
• In OW, not enough
power
• But same direction of
enrichment for
frugivores
How phenotypes evolve
Hayden, Dávalos et al. In Review Mol Biol Evol

42. Where is this going?
• Whole-transcriptome
survey of adaptive
convergence
• Target: energy
metabolism in nectar-feeding
bats
• Bottleneck: low quality
samples in collections
• Requires much
fieldwork
How phenotypes evolve

43. The limits of models
• In phylogenetics
• Models missing key biology
• Improving phylogenetic models
• How phenotypes evolve
!
• In environmental change
• Drivers of forest loss

44. My lab’s research mission
Biological
diversity
Diversificatio
n
Human
impact

45. Hamburger! (or steak)
Kaimowitz et al. 2004 CIFOR
Coca
Dávalos et al. 2011 Environ
Sci Technol
Land tenure and property
Hecht 1993 BioScience
Why do rainforests decline? Three hypotheses
Drivers forest loss

46. + demand beef
+ beef, + cattle
+ cattle, + pasture
+ pasture, - forest
Hamburger! (or steak)
Kaimowitz et al. 2004 CIFOR
Predictions
Coca
Dávalos et al. 2011 Environ
Sci Technol
Land tenure and property
Hecht 1993 BioScience
Drivers forest loss
+ demand cocaine
+ cocaine, + coca
+ coca, - forest
+ demand land
+ pasture, + cattle
+ cattle, - forest

47. Forest,
decrease coca nothing Eradication
The real drivers of
habitat loss
Urbanization
Development
Dávalos et al. 2009 Int J Drug Pol
Dávalos et al. In Review Biol Cons
becomes
Pasture
Cows
property is
Drivers forest loss

48. When models
mislead
• Models shape the kinds
of data we collect
• And how we interpret
those data
• Data may violate
model assumptions
• Data may reveal
underlying process
not captured by
model
• Models and data: a
dialogue

49. Thanks!
• Funding
• NSF–DEB, CIDER–SBU
• Speciation diversification: A. Cirranello,
A. Russell, N. Simmons, P. Velazco
• Functional evolution: E. Dumont, S.
Rossiter, E. Teeling
• Conservation policy: D. Armenteras, A.
Bejarano, A. Corthals, L. Correa, J.
Holmes, N. Rodriguez, C. Romero
• Dávalos Lab
• Phylogenetics: R. Dahan, S. DelSerra,
A. Goldberg, O. Warsi, L. Yohe, X.
Zhang
• Land use: P. Connell, M. Hall, E. Simola,
G. Tudda, Y. Shah
• Special thanks to staff: D. DiGiovanni, M.
Nolan, I. Roth, A. Stanley
• Colleagues for excellent dialogue
mentoring