1. Genetic & environmental contributions to a divergent plumage trait in barn swallows Joanna Hubbard, Amanda Hund, & Rebecca Safran University of Colorado Boulder Ecology & Evolutionary Biology Photo: Matt Wilkins

2. Hill 1992 Brawner et al 2000 Geographic Location Hill 1993 Genetic variation in biosynthetic pathway McGraw 2003 ♀ ♂ ♂

3. Rosenblum et al 2005 Nachman et al 2003 Theron et al 2001 Melanin-Based Color

4. Barn Swallow Species Complex

5. t 822.64 = -30.57; p < 0.001 Czech Republic North America

6. Nestling color is predictive of adult color Mechanism to maintain color throughout lifetime – Genotype or Developmental Plasticity? Hubbard et al in prep

7. How is phenotypic variation within populations influenced by genetic and environmental variation? How can we use this information to better understand reproductive isolation and the process of speciation?

8. Phenotypic Variation Genetic Variation Environmenta l Variation Unmeasured Variation Animal Model y i = µ + a i + e i + ε i a i = breeding value ei = environmental value

9. Site A Nest 1 Site B Nest 1 Reciprocal exchange Cross-Foster Nestlings Decouple genetic and environmental influences

10. Nests paired by: -Hatch date -Brood size (± 1) Swapped 90 nests (45 nest pairs) 56 control nests After Predation and Mortality: 494 Offspring; 107 Mothers; 96 Fathers Site A Nest 1 Site B Nest 1 Summer 2012: COSummer 2013: CZ Swapped 60 nests (30 nest pairs) 11 control nests After Predation and Mortality: 283 Offspring; 60 Mothers; 59 Fathers

11. Multivariate Animal Model Response Variables (standardized to the mean): 1.Brightness 2.Hue 3.Red Chroma Random effects 1.Pedigree – genetic variance 2.Nest ID – environmental variance

12. BrightnessHueChroma Heritability 0.1970.2000.156 (0.102 – 0.325)(0.106 – 0.376)(0.093 – 0.285) Environmental Influence 0.1680.2890.168 (0.120 – 0.280)(0.222 – 0.426)(0.110 – 0.266) Extra-Pair Paternity: ~35-40% (95% Bayesian Credible Interval – BCI) Colorado

13. Environmental Context e 2 ≅ 0.2 – 0.3 Female Preference h 2 ≅ 0.2 – 0.25

14. BrightnessHueChroma Heritability 0.2330.2070.247 (0.098 - 0.402)(0.109 - 0.406)(0.126 - 0.492) Environmental Influence 0.1920.2040.228 (0.102 - 0.291)(0.108 - 0.297)(0.116 - 0.335) Extra-Pair Paternity: ~16% (95% Bayesian Credible Interval – BCI) Czech Republic

15. Phenotypic Variation Environmenta l Variation Genetic Variation Population 1 Population 2 h 2 is not directly comparable V A1 /V P1 ≅ V A2 /V P2 Compare genetic variance-covariance matrices Phenotypic Variation Environmenta l Variation Genetic Variation

16. The G-Matrix Trait 1 Breeding Value Trait 2 Breeding Value Trait 1 Breeding Value Trait 2 Breeding Value Breeding Value: how an individual’s genotype shifts it away from the mean phenotype

17. ColoradoCzech Republic Brightness & Red Chroma -0.759 (-0.889 - -0.513) Brightness & Hue -0.105 (-0.525 – 0.370) Red Chroma & Hue 0.122 (-0.336 - 0.554) Brightness & Red Chroma -0.843 (-0.977 - -0.004) Brightness & Hue -0.137 (-0.433 – 0.495) Red Chroma & Hue -0.081 (-0.559 – 0.327)

18. Comparative Quantitative Genetics CO 1,1 CO 2,1...CO 1,n... CO m,1 CO m,2...CO m, n CZ 1,1 CZ 2,1...CZ 1,n... CZ m,1 CZ m,2...CZB m, n alpha E1 Observed Randomized No Divergence Aguirre et al Heredity 2014

19. G-Matrix Comparison Lower BCIUpper BCI Observed00.203 Randomize d 00.006

20. Phenotypic Variation Environmental Variation Genetic Variation No divergence in covariance structure ? Selection A1 A2 A3A6 A5 A7 A9 A6A3 A8

21. Conclusions Melanin-based color variation is affected by environmental variation Divergent selection may have driven phenotypic divergence among barn swallow subspecies Photo: Matt Wilkins

22. Future Directions Identify pigmentation genes that associate with color variation within and across populations Identify specific environmental factors that influence coloration (Amanda Hund – Session 3C_306C – Visual Signaling on Monday)

23. Collaborators: Tomáš Albrecht 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 Undergraduate Assistants Site Owners Acknowledgments

24. Total Amount of pigment Ratio of pigment type

25. CO results - Social BrightnessHueChroma VAVA 0.20.2060.168 (0.1 - 0.361)(0.117 - 0.418)(0.1 - 0.329) VEVE 0.1920.3090.181 (0.126 - 0.328)(0.207 - 0.484)(0.107 - 0.301) VRVR 0.6790.4690.687 (0.534 - 0.802)(0.348 - 0.595)(0.563 - 0.828) VPVP 1.0831.0651.103 (0.969 - 1.269)(0.917 - 1.237)(0.968 - 1.266)

26. CO results - Genetic BrightnessHueChroma VAVA 0.2750.2310.291 (0.131 – 0.567)(0.129 – 0.473)(0.121 – 0.573) VEVE 0.2270.2340.270 (0.144 – 0.401)(0.135 – 0.361)(0.144 – 0.396) VRVR 0.5230.5710.499 (0.313 – 0.627)(0.426 – 0.723)(0.293 – 0.615) VPVP 1.0691.0911.056 (0.942 – 1.238)(0.977 – 1.263)(0.939 – 1.239)

27. CR results - social BrightnessHueChroma VAVA 0.2060.2290.321 (0.122 - 0.517)(0.121 - 0.519)(0.134 - 0.599) VEVE 0.1860.220.242 (0.11 - 0.37)(0.111 - 0.374)(0.128 - 0.422) VRVR 0.650.6360.556 (0.462 - 0.851)(0.472 - 0.835)(0.359 - 0.751) VPVP 1.1851.211.147 (0.992 - 1.411)(0.994 - 1.415)(0.962 - 1.381)

28. CR results - genetic BrightnessHueChroma VAVA 0.2350.2440.341 (0.138 - 0.574)(0.131 - 0.529)(0.162 - 0.67) VEVE 0.1840.1930.243 (0.119 - 0.38)(0.121 - 0.381)(0.13 - 0.43) VRVR 0.6030.6010.456 (0.421 - 0.826)(0.437 - 0.817)(0.272 - 0.676) VPVP 1.1961.2071.097 (0.99 - 1.42)(0.97 - 1.406)(0.928 - 1.363)