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Elevation affects extra-pair paternity but not a sexually selected plumage trait in dark-eyed juncos

  • Katie LaBarberaEmail author
  • Kia R. R. Hayes
  • Kelley E. Langhans
  • Eileen A. Lacey
Original Article

Abstract

Differences in environmental conditions are expected to generate distinct selective pressures favoring different phenotypes. For example, environmental conditions that affect the timing of breeding may influence opportunities for extra-pair copulations and thus the strength of sexual selection on males. To explore these relationships quantitatively, we compared breeding synchrony, rates of extra-pair paternity, and expression of a sexually selected plumage trait (the amount of white on the tail feathers) in populations of dark-eyed junco (Junco hyemalis) breeding at elevations from 1960 to 2660 m in California. Microsatellite parentage analysis revealed that extra-pair paternity rates varied by elevation, with intermediate elevations having the highest rate. Differences in breeding synchrony could not explain this variation. Extra-pair males had more tail white than the social males they cuckolded, consistent with tail white being a sexually selected trait. Although the observed differences in rates of extra-pair paternity suggested that sexually selected traits should also vary with elevation, there were no differences among elevations in the amount of white on male tails or in the correlation between tail white and proxies for male condition. Multiple factors may have contributed to this result, including persistent gene flow among elevations, which may counter the effects of local differences in selective pressures. These findings demonstrate the complexity of interactions among environmental conditions, selective pressures, and variation in phenotypic traits, and underscore the importance of assessing the impacts of sexual selection in the larger context of population genetic structure.

Significance statement

Environmental differences, such as those occurring along elevation gradients, can lead to differences in sexual selection. We found that juncos at mid elevations had higher rates of extra-pair paternity than juncos at high and low elevations. Our results also provide evidence that male tail plumage is sexually selected, as females preferred to copulate with males with more white on their tail plumage than the females’ social mates. This suggests that male tail white should differ among elevations, as the reproductive rewards of having an attractive tail would be greater at mid elevations. However, we found no differences in male tail white among elevations. This may be due to the birds breeding freely across elevations, as evidenced by a lack of genetic structure, i.e., gene flow swamping out any differences that might otherwise form.

Keywords

Breeding synchrony Dark-eyed junco Elevation Extra-pair paternity Sexual selection 

Notes

Acknowledgments

We thank S. Beissinger, L. Smith, J. P. Kelley, J. Scullen, and the San Francisco Bay Bird Observatory for the training and advice. The comments of three anonymous reviewers improved the manuscript. The following research assistants made important contributions to data collection: J. Bates, J. Carlisle, A. Gilbert, L. Hall, V. Kimzey, K. Lyberger, A. M. Lee, K. Marsh, S. Maclean, A. Misraraj, H. Park, J. Spool, J. Tseng, and J. Van Bourg.

Funding

This work was supported by a National Science Foundation Graduate Research Fellowship, a Berkeley Fellowship from UC Berkeley, Museum of Vertebrate Zoology funds, and grants from the American Ornithologists’ Union, the Animal Behavior Society, and Sigma Xi.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All procedures involving live birds were approved by UC Berkeley’s Animal Care and Use Committee (protocol #R317–0815) and performed under the appropriate federal, state, and local permits.

Supplementary material

265_2019_2698_MOESM1_ESM.docx (104 kb)
ESM 1 (DOCX 104 kb)

References

  1. Ardia D (2005) Super size me: an experimental test of the factors affecting lipid content and the ability of residual body mass to predict lipid stores in nestling European Starlings. Funct Ecol 19:414–420CrossRefGoogle Scholar
  2. Atwell JW, Cardoso GC, Whittaker DJ, Price TD, Ketterson ED (2014) Hormonal, behavioral, and life-history traits exhibit correlated shifts in relation to population establishment in a novel environment. Am Nat 184:E147–E160CrossRefGoogle Scholar
  3. Badyaev AV (1997) Altitudinal variation in sexual dimorphism: a new pattern and alternative hypotheses. Behav Ecol 8:675–690CrossRefGoogle Scholar
  4. Badyaev AV, Ghalambor CK (1998) Does a trade-off exist between sexual ornamentation and ecological plasticity? Sexual dichromatism and occupied elevational range in finches. Oikos 82:319–324CrossRefGoogle Scholar
  5. Badyaev AV, Ghalambor CK (2001) Evolution of life histories along elevational gradients: trade-off between parental care and fecundity. Ecology 82:2948–2960CrossRefGoogle Scholar
  6. Baker CM, Fox SF (1978) Dominance, survival, and enzyme polymorphism in dark-eyed juncos, Junco hyemalis. Evolution 32:697–711CrossRefGoogle Scholar
  7. Balenger SL, Johnson LS, Mays HL Jr, Masters BS (2009) Extra-pair paternity in the socially monogamous mountain bluebird Sialia currucoides and its effect on the potential for sexual selection. J Avian Biol 40:173–180CrossRefGoogle Scholar
  8. Balph MH, Balph DF, Romesburg HC (1979) Social status signaling in winter flocking birds: an examination of a current hypothesis. Auk 96:78–93Google Scholar
  9. Birkhead TR, Biggins JD (1987) Reproductive synchrony and extra-pair copulation in birds. Ethology 74:320–334CrossRefGoogle Scholar
  10. Bolnick DI, Nosil P (2007) Natural selection in populations subject to a migration load. Evolution 61:2229–2243CrossRefGoogle Scholar
  11. Bonier F, Eikenaar C, Martin PR, Moore IT (2014) Extrapair paternity rates vary with latitude and elevation in emberizid sparrows. Am Nat 183:54–61CrossRefGoogle Scholar
  12. Boves TJ, Buehler DA, Wood PB, Rodewald AD, Larkin JL, Keyser PD, Wigley TB (2014) Multiple plumage traits convey information about age and within-age-class qualities of a canopy-dwelling songbird, the Cerulean Warbler. Auk 131:20–31CrossRefGoogle Scholar
  13. Boyce AJ, Martin TE (2019) Interspecific aggression among parapatric and sympatric songbirds on a tropical elevational gradient. Behav Ecol 30:541–547CrossRefGoogle Scholar
  14. Boyle WA, Sandercock BK, Martin K (2016) Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta-analysis. Biol Rev 91:469–482CrossRefGoogle Scholar
  15. Breheny P, Burchett W (2017) Visualization of regression models using visreg. R J 9:56–71CrossRefGoogle Scholar
  16. Candolin U, Vlieger L (2013) Estimating the dynamics of sexual selection in changing environments. Evol Biol 40:589–600CrossRefGoogle Scholar
  17. Candolin U, Salesto T, Evers M (2007) Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 20:233–239CrossRefGoogle Scholar
  18. Cardoso GC, Atwell JW, Hu Y, Ketterson ED, Price TD (2012) No correlation between three selected trade-offs in birdsong performance and male quality for a species with song repertoires. Ethology 118:584–593CrossRefGoogle Scholar
  19. Chaine AS, Lyon BE (2008) Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319:459–462CrossRefGoogle Scholar
  20. Cleasby IR, Nakagawa S (2012) The influence of male age on within-pair and extra-pair paternity in passerines. Ibis 154:318-324CrossRefGoogle Scholar
  21. Clutton-Brock TH (2007) Sexual selection in males and females. Science 318:1882–1885CrossRefGoogle Scholar
  22. Clutton-Brock TH, Rose KE, Guinness FE (1997) Density-related changes in sexual selection in red deer. Proc R Soc Lond B 264:1509–1516CrossRefGoogle Scholar
  23. Corbitt C, Deviche P (2005) Age-related differences in size of brain regions for song learning in adult male dark-eyed juncos (Junco hyemalis). Brain Behav Evol 65:268–277CrossRefGoogle Scholar
  24. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/ Google Scholar
  25. de Kort S, Eldermire ERB, Valderrama S, Botero CA, Vehrencamp SL (2009) Trill consistency in an age-related assessment signal in banded wrens. Proc R Soc Lond B 276:2315–2321CrossRefGoogle Scholar
  26. de Zwaan DR, Greenwood JL, Martin K (2017) Feather melanin and microstructure variation in dark-eyed junco Junco hyemalis across an elevational gradient in the Selkirk Mountains. J Avian Biol 48:552–562CrossRefGoogle Scholar
  27. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefGoogle Scholar
  28. Enstrom DA, Ketterson ED, Nolan V (1997) Testosterone and mate choice in the dark-eyed junco. Anim Behav 54:1135–1146CrossRefGoogle Scholar
  29. Ferree ED (2007) White tail plumage and brood sex ratio in dark-eyed juncos (Junco hyemalis thurberi). Behav Ecol Sociobiol 62:109–117CrossRefGoogle Scholar
  30. Ferree ED (2013) Geographic variation in morphology of dark-eyed juncos and implications for population divergence. Wilson J Ornithol 125:454–470CrossRefGoogle Scholar
  31. Freckleton RP (2002) On the misuse of residuals in ecology: regression of residuals vs multiple regression. J Anim Ecol 71:542–545CrossRefGoogle Scholar
  32. Gosden TP, Svensson EI (2008) Spatial and temporal dynamics in a sexual selection mosaic. Evolution 62:845–856CrossRefGoogle Scholar
  33. Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proc R Soc Lond B 251:111–117CrossRefGoogle Scholar
  34. Grunst ML, Grunst AS, Gonser RA, Tuttle EM (2017) Breeding synchrony and extrapair paternity in a species with alternative reproductive strategies. J Avian Biol 48:1087–1094CrossRefGoogle Scholar
  35. Guisan A, Edwards TC Jr, Hastie T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model 157:89–100CrossRefGoogle Scholar
  36. Habel JC, Ulrich W, Peters G, Husemann M, Lens L (2014) Lowland panmixia versus highland disjunction: genetic and bioacoustic differentiation in two species of East African White-eye birds. Conserv Genet 15:655–664CrossRefGoogle Scholar
  37. Haldane JBS (1930) A mathematical theory of natural and artificial selection. (part VI, isolation.). Math Proc Cambridge 26:220–230CrossRefGoogle Scholar
  38. Hastie T, Tibshirani R (1986) Generalized additive models. Stat Sci 1:297–318CrossRefGoogle Scholar
  39. Helms CW, Aussiker WH, Bower EB, Fretwell SD (1967) A biometric study of major body components of the Slate-colored Junco, Junco hyemalis. Condor 69:560–578CrossRefGoogle Scholar
  40. Hill JA, Enstrom DA, Ketterson ED, Nolan V, Ziegenfus C (1999) Mate choice based on static versus dynamic secondary sexual traits in the dark-eyed junco. Behav Ecol 10:91–96CrossRefGoogle Scholar
  41. Holberton RL, Able KP, Wingfield JC (1989) Status signalling in dark-eyed juncos, Junco hyemalis: plumage manipulations and hormonal correlates of dominance. Anim Behav 37:681–689CrossRefGoogle Scholar
  42. Ims RA (1990) The ecology and evolution of reproductive synchrony. Trends Ecol Evol 5:135–140CrossRefGoogle Scholar
  43. Johnson A, Lifjeld JT (2003) Ecological constraints on extra-pair paternity in the bluethroat. Oecologia 136:476–483CrossRefGoogle Scholar
  44. Johnson LS, Brubaker JL, Ostlind E, Balenger SL (2007) Effect of altitude on male parental expenditure in Mountain Bluebirds (Sialia currucoides): are higher-altitude males more attentive fathers? J Ornithol 148:9–16CrossRefGoogle Scholar
  45. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefGoogle Scholar
  46. Kempanaers B (1993) The use of a breeding synchrony index. Ornis Scand 24:84CrossRefGoogle Scholar
  47. Ketterson ED (1979) Aggressive behavior in wintering dark-eyed juncos: determinants of dominance and their possible relation to geographic variation in sex ratio. Wilson Bull 91:371–383Google Scholar
  48. Ketterson ED, Parker PG, Raouf SA, Nolan V, Ziegenfus C, Chandler CR (1998) The relative impact of extra-pair fertilizations on variation in male and female reproductive success in dark-eyed juncos (Junco hyemalis). Ornithol Monogr (49):81–101Google Scholar
  49. Kwiatkowski MA, Sullivan BK (2002) Geographic variation in sexual selection among populations of an iguanid lizard, Sauromalus obesus (=ater). Evolution 56:2039–2051CrossRefGoogle Scholar
  50. LaBarbera K, Lacey EA (2018) Breeding season length and nest mortality drive cryptic life history variation in dark-eyed juncos (Junco hyemalis) breeding across a montane elevation gradient. Auk 135:284–298CrossRefGoogle Scholar
  51. LaBarbera K, Llambías PE, Cramer ERA, Schaming TD, Lovette IJ (2010) Synchrony does not explain extrapair paternity rate variation in northern or southern house wrens. Behav Ecol 21:773–780CrossRefGoogle Scholar
  52. Martín J, López P (2009) Multiple color signals may reveal multiple messages in male Schreiber’s green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63:1743–1755CrossRefGoogle Scholar
  53. McGlothlin JW, Parker PG, Nolan V, Ketterson ED (2005) Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos. Evolution 59:658–671CrossRefGoogle Scholar
  54. McGlothlin JW, Duffy DL, Henry-Freeman JL, Ketterson ED (2007) Diet quality affects an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 61:1391–1399CrossRefGoogle Scholar
  55. Nolan V, Ketterson ED, Cristol DA, Rogers CM, Clotfelter ED, Titus RC, Schoech SJ, Snajdr E (2002) Dark-eyed junco (Junco hyemalis). In: Poole A (ed) The birds of North America online, Cornell Lab of Ornithology, Ithaca, bna.birds.cornell.edu/bna/species/716
  56. Pakanen VM, Orell M, Vatka E, Rytkönen S, Broggi J (2016) Different ultimate factors define timing of breeding in two related species. PLoS One 11:e0162643CrossRefGoogle Scholar
  57. Price TD, Yeh PJ, Harr B (2008) Phenotypic plasticity and the evolution of a socially selected trait following colonization of a novel environment. Am Nat 172:S49–S62CrossRefGoogle Scholar
  58. Punzalan D, Rodd FH, Rowe L (2010) Temporally variable multivariate sexual selection on sexually dimorphic traits in a wild insect population. Am Nat 175:401-414CrossRefGoogle Scholar
  59. Rice WR, Gaines SD (1994) ‘Heads I win, tails you lose’: testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol Evol 9:235–237CrossRefGoogle Scholar
  60. Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2008) Environmental heterogeneity generates fluctuating selection on a secondary sexual trait. Curr Biol 18:751–757CrossRefGoogle Scholar
  61. Santos RG, Pinheiro HT, Martins AS, Riul P, Bruno SC, Janzen FJ, Ioannou CC (2016) The anti-predator role of within-nest emergence synchrony in sea turtle hatchlings. Proc R Soc B 283:20160697CrossRefGoogle Scholar
  62. Schmoll T (2011) A review and perspective on context-dependent genetic effects of extra-pair mating in birds. J Ornithol 152:265–277CrossRefGoogle Scholar
  63. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefGoogle Scholar
  64. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass–size residuals: validating body condition indices. Ecology 86:155–163CrossRefGoogle Scholar
  65. Stutchbury BJM (1998) Breeding synchrony best explains variation in extra-pair mating system among avian species. Behav Ecol Sociobiol 43:221–222CrossRefGoogle Scholar
  66. Stutchbury BJ, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690CrossRefGoogle Scholar
  67. Taff CC, Freeman-Gallant CR, Dunn PO, Whittingham LA (2013) Spatial distribution of nests constrains the strength of sexual selection in a warbler. J Evol Biol 26:1392–1405CrossRefGoogle Scholar
  68. Terborgh J (1971) Distribution on environmental gradients: theory and a preliminary interpretation of distributional patterns in avifauna of Cordillera Vilcabamba, Peru. Ecology 52:23–40CrossRefGoogle Scholar
  69. Weatherhead PJ, Yezerinac SM (1998) Breeding synchrony and extra-pair mating in birds. Behav Ecol Sociobiol 43:217–219CrossRefGoogle Scholar
  70. Webster MS, Pruett-Jones S, Westneat DF (1995) Measuring the effects of pairing success, extra pair copulations and mate quality on the opportunity for sexual selection. Evolution 49:1147–1157CrossRefGoogle Scholar
  71. Webster MS, Tarvin KA, Tuttle EM, Pruett-Jones S (2007) Promiscuity drives sexual selection in a socially monogamous bird. Evolution 61:2205–2211CrossRefGoogle Scholar
  72. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Ann Rev Ecol Evol S 34:365–396CrossRefGoogle Scholar
  73. Westneat DF, Sherman PW, Morton ML (1990) The ecology and evolution of extra-pair copulations in birds. Curr Ornithol 7:331–369Google Scholar
  74. Wolf WL, Casto JM, Nolan V, Ketterson ED (2004) Female ornamentation and male mate choice in dark-eyed juncos. Anim Behav 67:93–102CrossRefGoogle Scholar
  75. Wood SN (2008) Fast stable direct fitting and smoothness selection for generalized additive models. J Roy Stat Soc B 70:495–518CrossRefGoogle Scholar
  76. Wood SN (2017) Generalized additive models: an introduction with R, 2nd edn. CRC/Taylor and Francis, Boca RatonCrossRefGoogle Scholar
  77. Yeh PJ, Price TD (2004) Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am Nat 164:531–542CrossRefGoogle Scholar
  78. Yezerinac SM, Weatherhead PJ, Boag PT (1995) Extra-pair paternity and the opportunity for sexual selection in a socially monogamous bird (Dendroica petechia). Behav Ecol Sociobiol 37:179–188CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Museum of Vertebrate ZoologyUniversity of California - BerkeleyBerkeleyUSA
  2. 2.Institute of Environmental and Human HealthLubbockUSA
  3. 3.Department of BiologyStanford UniversityStanfordUSA

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