From Micro to Macro: The Evolution
of Phenotypic Diversity in Plethodon
Salamanders
Dean C. Adams
Department of Ecology, Evolution and
Organismal Biology
Department of Statistics
Iowa State University
Understanding Phenotypic Diversification
•How do evolutionary processes at one temporal scale affect patterns
of diversity at other scales?
•Species interactions often drive diversity at contemporary timescales
•Such patterns are not always seen at the macroevolutionary level
(Jablonski 2008)
•Theoretical approaches linking micro- and macroevolution also
remain underdeveloped
•Therefore, how do we study the link between the two?
From Micro- and Macroevolution: I
•How do taxa and populations respond to similar selective pressures?
•Sometimes similar responses are found to common selection
pressures (e.g., Schluter and McPhail, 1992; Reznick et al. 1996; Losos et al. 1998)
•Strong evidence of adaptation, and suggests a link between
microevolutionary change and macroevolutionary diversification
•This begs the question:
To what extent is the evolutionary process ‘repeatable’?
•To assess this question requires two things:
1: A method to quantify patterns of phenotypic evolution
2: Statistically comparing patterns across replicated evolutionary units
4
Quantifying Phenotypic Evolution
2
V3
3
Y2
Yi
0
1
Y1
0
1
2
3
4
0
1
2
3
4
V2
V1
•Phenotypic evolution is a trajectory in morphospace
•Evolutionary trajectories completely defined by attributes:
p3
•Magnitude
Y
•Orientation
2
•Shape
Collyer and Adams. 2007. Ecology. 88:683-692.
p1
p2
Adams and Collyer. 2007. Evolution. 61:510-515.
Adams and Collyer. 2009. Evolution. 63:1143-1154.
Comparing Evolutionary Trajectories
•Quantify trajectory attributes
Phenotypic Evolution Vector
Magnitude

 y11  y12 


Yi  (Y1  Y 2 )   y 21  y 22 


 y 31  y 32 
T
i
DEi   Y  Yi
Shape
Direction

1/ 2
  cos 1 r
r
MD  DEi  DEj
YT i Yj
DEi DEj
DPr oc ij 
Y
npi - Ynpj 
2
Note: Trajectory shape only used
when trajectories have 3+ levels
•Statistically evaluate using residual randomization
4
Y j
Summary Stat
3
m m 1 /2
VarSize 
2
V3


 
 m  m  1 / 2   1
MDi  MD
2
i
0
1
Yi
0
1
2
3
V1
4
0
1
2
3
4
V2
Collyer and Adams. 2007. Ecology. 88:683-692.
Adams and Collyer. 2007. Evolution. 61:510-515.
Adams and Collyer. 2009. Evolution. 63:1143-1154.
Phenotypic Variation in Plethodon
•Natural, replicated evolutionary experiment
•55 species; 105 different community combinations (1-5 spp)
•Different geographic attributes (narrow/broad,
stable/shifting) and competitive interactions
•Geography, genetics, phylogenetics, behavior, and
ecological requirements well documented
•Many studies reveal phenotypic changes
associated with competition
See:
Adams 2000. in Biol. Pleth. Salamanders. 383-394.
Adams and Rohlf. 2000. PNAS. 97:4106-4111.
Adams. 2004. Ecology. 85:2664-2670.
Maerz, Myers, and Adams. 2006. Evol. Ecol. Res. 8:23-35.
Adams et al 2007. J. Anim. Ecol. 76:289-295.
Arif, Adams, Wicknick. 2007. Evol. Ecol. Res. 9:843-854.
Myers and Adams. 2008. Herpetologica. 64:281-289.
Salamander images from Petranka, 1998.
Example 1: P. jordani & P. teyahalee
•Extensive ecological work demonstrates competition prevalent
•Character displacement in head shape observed (Adams 2004)
•Head shape associated with aggressive behavior (Adams 2004)
•Species come into contact in several distinct locations
Question:
•Are microevolutionary patterns repeatable across the distributions of
these species?
Adams 2009. Am. Nat. (In Review).
Example 1: P. jordani & P. teyahalee
•336 specimens from 3 independent geographic transects
•Head shape quantified using GMM
•Evolutionary vectors (allopatrysympatry) quantified and compared
Adams 2009. Am. Nat. (In Review).
Example 1: P. jordani & P. teyahalee
•Patterns suggest phenotypic evolution resulting from competition
Factor
DfFactor
Pillai’s Trace
Approx. F df
P
Species
1
0.741
48.874
18, 307
< 0.0001
Locality Type
1
0.794
65.612
18, 307
< 0.0001
Geographic Transect
2
0.783
11.015
36, 616
< 0.0001
Species × Locality
1
0.519
18.373
18, 307
< 0.0001
Species × Transect
2
0.289
2.888
36, 616
< 0.0001
Locality × Transect
2
0.338
3.482
36, 616
< 0.0001
Species×Locality×Transect
2
0.161
1.499
36, 616
0.0327
Adams 2009. Am. Nat. (In Review).
Example 1: P. jordani & P. teyahalee
•NO difference in magnitude or direction of evolutionary changes
among transects within species (i.e. common patterns found)
•Conclusion: Evolutionary response to competition repeatable in each
species: parallel evolution of character displacement
Adams 2009. Am. Nat. (In Review).
From Micro- and Macroevolution: II
•Competition among Plethodon species prevalent
•Competition frequently associated with phenotypic evolution
•Do microevolutionary changes from competition generate adaptive
diversification across lineages?
•If competitive adaptive diversification, we expect:
•Association of phenotypic variation and community type
•Phylogenetic association of phenotype and community
•Early dispersion of phenotypic evolution in morphospace
•Greater disparity through time relative to chance
•Requires a phylogenetic perspective
Example 2: P. cinereus Clade
•465 specimens from 52 populations
of 8 species (P. sherando & P.serratus not
P. virginia
included)
P. hoffmani
•Chronogram from tree of Highton
(1999: Herpetologica): calibrated
branch points from Wiens et al. (2006:
Evolution)
•GLS: Morphological variation vs. community
composition
•Within-species morphological disparity
examined
•PGLS: Morphological variation vs. community
composition (phylogeny constant)
•Disparity through time (vs. expectation via
Brownian motion simulations)
P. electromorphus
P. richmondi
P. nettingi
P. hubrichti
P. serratus
P. cinereus
10.0
8.0
6.0
4.0
MYA
2.0
0.0
Adams & Collyer (unpublished).
Example 2: P. cinereus Clade
•Phenotypic diversity affected by phylogeny
Phylogenetically naïve
Phylogenetically informed
•Community effect stronger once phylogeny is accounted for
PGLS parameter
estimates
LS parameter estimates
0L,1S
PC
II
1L,2S
2L,1S
1L,1S
0L,1S
2L,2S 0L,2S
2L,2S
2L,1S
1L,2S
1L,1S
0L,2S
PC I
PC I
PC I
Adams & Collyer (unpublished).
Example 2: P. cinereus Clade
•Early nodes show significant disparity (adaptive signal)
•‘Repulse’ one another in morphospace (indicative of competition)
P. v.
Present
P. ho.
2 MYA
4 MYA
P. e.
6 MYA
P. r.
0.00
-0.04
-0.04
P. n.
P. hu.
P. s.
0.04
8 MYA
0.00
PC II
P. c.
0.04
PC I
10.0
8.0
6.0
4.0
MYA
2.0
0.0
Adams & Collyer (unpublished).
Example 2: P. cinereus Clade
1.0
0.5
Observed Disparity
0.0
Relative Disparity (within subclades)
1.5
•Significantly greater within-group disparity than expected by chance
Random (Brownian)
0.0
0.2
0.4
0.6
0.8
1.0
Time
•Microevolutionary changes do not result in phenotypic novelties
•Suggests recurrent evolution and morphological homoplasy
through time
Adams & Collyer (unpublished).
Conclusions
•Some links between micro- and macroevolution can be assessed
•Replicated patterns (example 1)
•Phylogenetic trends (example 2)
•Rates of evolution (e.g., Adams et al. 2009: Proc. Roy. Soc.)
•Phylogenetic convergence/parallelism (e.g., Revell et al. 2007: Evol.)
•Models of evolution (e.g., Butler and King 2004: Am. Nat.)
•Additional analytical methods need to be developed
Acknowledgments
Previous Lab Members
Dr. Michael Collyer (Postdoc 2003-2007)
Saad Arif (MS: 2005)
Kara Butterworth (MS: 2003)
Dr. Melinda Cerney (PhD: 2005)
Dr. Jennifer Deitloff (PhD: 2008)
Jennifer Donnelly (MS: 2003)
Aspen Garry (MS: 2003)
Dr. Erin Myers (PhD: 2008)
Ashley Connor (undergraduate)
Julie Perrett (undergraduate)
Nicole Seda (undergraduate)
Audri Weaver (undergraduate)
Mary West (undergraduate)
Kate Weigert (undergraduate)
Meredith Zipse (undergraduate)
Funding
NSF DEB-0122281
NSF CAREER DEB-0446758
& Supplements
Current Lab Members
Chelsea Berns (PhD student)
Jim Church (PhD student)
Andrew Kraemer (PhD student)
USNM (esp. A. Wynn)