Early nest environment and genes have lifetime

effects on the expression of a colorful sexual signal

Joey K. Hubbard, Brittany R. Jenkins, Rebecca J. SafranJoanna.Hubbard@colorado.edu

Animal Behavior SocietyJuly 30, 2013

Phenotypic Variation

GenesSelective pressure

Phenotypic change over generations

EnvironmentEnvironmental change

Phenotypic change over a short time

period

Sexually-Selected Traits

Phenotypic Variation

Environmental Control

Genetic Control

Indirect Benefits

Direct Benefits

Colorful Plumage Traits

Melanin-Based Color

North American Barn Swallows

• Sexual trait• Socially

Monogamous• Extra-pair

paternity

• Monitoring Boulder County breeding population since 2008

Safran & McGraw 2004; Safran et al. 2005

Determined paternity using microsats

Pedigree530 offspring with 111 mothers and 98 fathers

Animal Model

• Univariate animal model to partition sources of variance for each color descriptor

• Determine key variance components• Calculate variance ratios

VP = VA + VT + VCE + VME + VR

Variance Ratios

h2 VA/VP: Narrow sense heritability

t2 VT/VP: Effect of seasonal variation

ce2 VCE/VP: Effect of common environment

me2 VME/VP: Effect of maternal environment

VP = VA + VT + VCE + VME + VR

Influences on Juvenile Color

Variance Ratios Avg. Brightness

h2

heritability 0.10 (0.23)

t2

seasonal effect 0.05 (0.04)

ce2

common environment

0.11 (0.08)

me2

maternal environment

0.05 (0.09)

Hubbard et al. in prep(Standard Error)

Influences on Juvenile Color

Variance Ratios Avg. Brightness Hue

h2

heritability 0.10 (0.23) 1.1-07 (7.1e-09)

t2

seasonal effect 0.05 (0.04) 0.03 (0.04)

ce2

common environment

0.11 (0.08) 0.09 (0.08)

me2

maternal environment

0.05 (0.09) 0.12 (0.07)

Hubbard et al. in prep(Standard Error)

Influences on Juvenile Color

Variance Ratios Avg. Brightness Hue Chroma

h2

heritability 0.10 (0.23) 1.1-07 (7.1e-09) 0.19 (0.15)

t2

seasonal effect 0.05 (0.04) 0.03 (0.04) 0.05 (0.04)

ce2

common environment

0.11 (0.08) 0.09 (0.08) 0.13 (0.08)

me2

maternal environment

0.05 (0.09) 0.12 (0.07) 4.3-07 (7.5e-08)

Hubbard et al. in prep(Standard Error)

Within-Individual Variation

Hatch Year Second Year

Year 1 Year 2

54 individuals(out of ~4000 nestlings)

205 individuals

Within-Individual Variation

Hatch Year Second Year

Within-Individual Variation

b R2 pBrightness 0.48 0.22 <

0.001Hue 0.10 0 0.49

Chroma 0.87 0.29 < 0.001

Hatc

h Ye

ar to

Seco

nd Y

ear

Within-Individual Variation

b R2 pBrightness 0.48 0.22 <

0.001Hue 0.10 0 0.49

Chroma 0.87 0.29 < 0.001

b R2 pBrightness 0.41 0.21 <

0.001Hue 0.21 0.04 0.003

Chroma 0.53 0.30 < 0.001

Year

1 to

Ye

ar 2

Hatc

h Ye

ar to

Seco

nd Y

ear

Summary

Genetic Variation

Environmental Variation

Maternal Environment

✔ ✔

For the Swallows

• Early environment has long-term effects on signal development

• Females gain both indirect and direct benefits

Heritability Estimates

Ignoring other sources of non-independence results in overestimation of heritability

AM with environment

AM no environment

P-O Regression

Sibling Correlation

h2 = 0.10 h2 = 0.45 h2 = 0.36 h2 = 0.84

Average Brightness

Cross-fostering experiments

• Experimentally tease apart effects of shared genes and shared environment

• Explore specific environmental influences

Thanks!

Funding:American Ornithologists UnionAnimal Behavior SocietyCU EBIO DepartmentCU Graduate SchoolNSFCU BURST and UROP programs

Lab and Field Help:Amazing Field Crews! Site OwnersStephen Alderfer Monica BrandhuberAndrew Flynn Amanda HundEric Lord Julie MarlingLiz Scordato Audrey TobinTy Tuff Courtney van der LindenRachel Wildrick Matt Wilkins

Photo Credit:Matt WilkinsIan Harold

Quantitative GeneticsVariance

Components Avg. Brightness Hue Chroma

Trait Mean 29.98% (0.015) 618.94 nm (0.04) 0.41 (5.04e-5)

VA5.91 (12.82)

p = 0.6965.23e-05 (3.81e-06)

p = 0.9991.16e-04 (9.44e-05)

p = 0.326

VT2.97 (2.55)

p = 016.87 (20.15)

p = 0.3623.11e-05 (2.63e-05)

p = 0.167

VCE6.46 (4.57)p = 0.125

41.56 (38.22)p = 0.263

7.63e-05 (4.80e-05)p = 0.090

VME2.57 (5.39)p = 0.664

60.92 (35.40)p = 0.088

2.63e-10 (4.43e-11)p = 0.999

VR 38.92 (8.14) 369.60 (26.93) 3.86e-04 (6.50e-05)

VP 56.84 (0.303) 488.95 (0.088) 6.09e-04 (1.06e-04)