Genetic & environmental contributions to a divergent plumage trait in barn swallows

Joanna Hubbard, Amanda Hund, Tomas Albrecht, & Rebecca Safran

University of Colorado BoulderEcology & Evolutionary BiologyPhoto: Matt Wilkins

Hill 1992

Brawner et al 2000Geographic

Location

Hill 1993

Genetic variation in biosynthetic

pathway

McGraw 2003

♀

♂♂

Rosenblum et al 2005Nachman et al 2003

Theron et al 2001

Melanin-Based Color

Barn Swallow Species Complex

Tetrahedral Color Space

Stoddard & Prum. 2008. Am Nat

Cou

nt

North America Czech Republic

• Nestling color is predictive of adult color

• Mechanism to maintain color throughout lifetime– Genotype or Developmental Plasticity?

Hubbard et al in review

Site ANest 1

Site BNest 1

Reciprocal exchange

Cross-Foster Nestlings

Decouple genetic and environmental

influences

Nests paired by:- Hatch date- Brood size (± 1)

Swapped 90 nests(45 nest pairs)

56 control nests

After Predation and Mortality:

431 Offspring(211 WPY, 189 EPY,

31?)

Site ANest 1

Site BNest 1

Summer 2012: CO Summer 2013: CZ

Swapped 60 nests(30 nest pairs)

11 control nests

After Predation and Mortality:

283 Offspring(227 WPY, 47 EPY, 9

P)

Multivariate Animal Model

Random effects• Pedigree• Nest Origin • Nest Reared

Phenotypic Variation

Genetic Variation

Environmental Variation

UnmeasuredVariation

Early Environmen

t

Rearing Environmen

t

Response Variables• Theta• Phi• r Achieved• Brightness

(95% Bayesian Credible Interval – BCI)

Theta Phi r Achieved Brightness

Heritability0.163 0.161 0.165 0.172

(0.132 - 0.205)

(0.133 - 0.205)

(0.132 - 0.206)

(0.136 - 0.210)

Early Environment

0.373 0.352 0.328 0.356(0.281 - 0.421)

(0.281 - 0.427)

(0.282 - 0.426)

(0.271 - 0.418)

Rearing Environment

0.359 0.35 0.347 0.347(0.274 - 0.416)

(0.269 - 0.413)

(0.273 - 0.417)

(0.266 - 0.410)

Heritability0.149 0.153 0.149 0.161

(0.112 - 0.195)

(0.111 - 0.197)

(0.107 - 0.198)

(0.115 - 0.207)

Early Environment

0.354 0.367 0.352 0.318(0.262 - 0.461) (0.262 - 0.46) (0.255 -

0.459)(0.248 - 0.449)

Rearing Environment

0.361 0.383 0.359 0.364

(0.27 - 0.463) (0.267 - 0.464)

(0.263 - 0.471)

(0.266 - 0.467)

EnvironmentalContext

e2 ≅ 0.32 - 38Selection

h2 ≅ 0.15 - 17

Population 1 Population 2

h2 is not directly comparable

VA1/VP1 ≅ VA2/VP2

Phenotypic Variation

Genetic Variation

Environmental Variation

Phenotypic Variation

Genetic Variation

Environmental Variation

Compare genetic variance-covariance matrices

The G-Matrix

Trait 1 Breeding Value

Trait

2 B

reedin

g V

alu

e

Trait 1 Breeding ValueTr

ait

2 B

reedin

g V

alu

e

Breeding Value: how an individual’s genotype shifts it away from the mean phenotype

Comparative Quantitative Genetics

CO1,1 CO2,1 ... CO1,n

... ... ... ...

COm,1 COm,2 ... COm,n

CZ1,1 CZ2,1 ... CZ1,n

... ... ... ...

CZm,1 CZm,2 ... CZBm,n

alp

ha

E1 E1

ObservedRandomized

NoDivergence Divergence

Aguirre et al Heredity 2014

G-Matrix Comparison

Lower BCI Upper BCI

Observed 3.9 x 10-5 2.67 x 10-

4

Randomized 0 8 x 10-6

Brightness contributes to this difference more so

than other color metrics

Phenotypic Variation

Environmental Variation

Genetic Variation

Divergence in covariance structure

?

Selection

A1A2

A3 A6

A5A7

A9A6 A3

A8

Conclusions• Melanin-based color variation is affected

by environmental variation with low heritability

• Divergent selection on plumage brightness will increase phenotypic differences

• Divergent selection may have led to current phenotypic differences

Photo: Matt Wilkins

Future Directions

• Identify pigmentation genes that associate with color variation within and across populations

• Include additional subspecies and incorporate comparative phylogenetic methods

• Identify specific environmental factors that influence coloration

Collaborators:

• Adela Petrželková

• Romana Michálková

• Martina Soudková

• Olda Tomášek

• Natália Prekopová

• Lucie Jančíková

Funding:• EBIO department• CU Graduate School• Animal Behavior Society• American Ornithologists’

Union• American Museum of Natural

History• Colorado Field Ornithologists

• Max Joseph• Matt Wilkins• Liz Scordato• David Zonana• Iris Levin• Undergraduate Assistants• Site Owners

Acknowledgments