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Multiple sexual pigments, assortative social pairing, and genetic paternity in the yellow warbler (Setophaga petechia)

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Abstract

In socially monogamous species, extra-pair paternity may increase the reproductive success of highly ornamented males, mediating the evolution of sexual ornaments. However, ornaments may also attract social mates, and a tradeoff between extra-pair paternity (EPP) and within-pair paternity (WPP) may complicate mating strategies. Further, in many socially monogamous species, females are also ornamented, and the relationship between female ornamentation and patterns of EPP has been neglected. We investigated the patterns of genetic paternity with respect to carotenoid- and melanin-based pigmentation in yellow warblers (Setophaga petechia) of both sexes. We asked whether males face tradeoffs between EPP and WPP, how paternity patterns relate to carotenoid- versus melanin-based pigmentation, and whether less EPP occurs in broods when males and females are assortatively paired. Males faced a tradeoff between EPP and WPP. Moreover, non-additive relationships existed between paternity patterns and the two pigment types in both sexes. Males with high melanin coverage but dull carotenoid pigmentation achieved EPP but lost WPP, whereas males with high levels of both pigment types had high WPP but gained little EPP. A parallel pattern occurred in females. Warblers paired assortatively by pigmentation and EPP was less common in broods when the sexes were assortatively paired by carotenoid pigmentation. Results suggest that the most colorful birds obtain high quality social mates and advance reproductive success through WPP, show that correlations can arise between female ornamentation and patterns of EPP, and also uniquely suggest that social pairing patterns may influence extra-pair mating strategies.

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References

  • Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155

    Article  PubMed  Google Scholar 

  • Andersson M, Prager M (2006) Quantifying color. In: Hill G, McGraw K (eds) Bird coloration, vol 1, Mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147

    Google Scholar 

  • Balenger S, Johnson LS, Masters B (2009) Sexual selection in a socially monogamous bird: male color predicts paternity in the mountain blue bird, Sialia currucoides. Behav Ecol Sociobiol 63:403–411

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0. http://CRAN.R-project.org/package=lme4

  • Bouwman KM, Komdeur J (2006) Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus. J Avian Biol 37:238–244

    Article  Google Scholar 

  • Canal D, Jovani R, Potti D (2012) Male decisions or female accessibility? Spatiotemporal patterns of extrapair paternity in a songbird. Behav Ecol 23:1146–1153

    Article  Google Scholar 

  • Chuang-Dobbs HC, Webster MS, Holmes RT (2001) The effectiveness of mate guarding by male black-throated blue warblers. Behav Ecol 12:541–546

    Article  Google Scholar 

  • Crary A, Rodewald R (2012) Plumage coloration and ornamentation as predictors of nest survival and number of young fledged in yellow warblers. J Field Ornithol 83:130–140

    Article  Google Scholar 

  • Dawson R, Gibbs H, Hobson K, Yezerinac S (1997) Isolation of microsatellite DNA markers from a passerine bird, Dendroica petechia (the yellow warbler), and their use in population studies. Heredity 79:506–514

    Article  CAS  PubMed  Google Scholar 

  • Delhey K, Johnsen A, Peters A, Andersson S, Kempenaers B (2003) Paternity analysis reveals opposing selective pressures on crown colour in blue tits (Parus caeruleus). Proc R Soc Lond B 270:2057–2053

    Article  Google Scholar 

  • Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration, and behavioral syndromes. Trends Ecol Evol 29:502–510

    Article  Google Scholar 

  • Ferretti V, Massoni V, Bulit F, Winkler DW, Lovette IJ (2011) Heterozygosity and fitness benefits of extrapair mate choice in white-rumped swallows (Tachycineta leucorrhoa). Behav Ecol 22:1178–1186

    Article  Google Scholar 

  • Fisherman MA, Stone L, Lotem A (2003) Fertilization insurance through extra-pair fertilization and male paternity defense. J Theor Biol 221:103–114

    Article  Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld J, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair mating. Nature 425:714–717

    Article  CAS  PubMed  Google Scholar 

  • Forstmeier W, Martin K, Bolund E, Schielzeth H, Kempenaers B (2011) Female extrapair behavior can evolve via indirect selection on males. Proc Natl Acad Sci U S A 108:10608–10613

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Freeman-Gallant C, Wheelwright N, Meiklejohn K, States S, Sollecito S (2005) Little effect of extrapair paternity on the opportunity for sexual selection in savannah sparrows (Passerculus sandwichensis). Evolution 59:422–430

    PubMed  Google Scholar 

  • Gowaty PC (1996) Battle of the sexes and the origins of monogamy. In: Black JM (ed) Partnerships in birds. Oxford University Press, Oxford, pp 21–52

    Google Scholar 

  • Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2211

    Article  CAS  PubMed  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  CAS  PubMed  Google Scholar 

  • Grunst AS, Rotenberry JT, Grunst ML (2014a) Age-dependent relationships between multiple sexual pigments and condition in males and females. Behav Ecol 35 (published online doi:10.1093/beheco/art124)

  • Grunst AS, Salgado-Ortiz J, Rotenberry JT, Grunst ML (2014b) Phaeomelanin- and carotenoid-based sexual pigmentation reflect oxidative status in two populations of the yellow warbler (Setophaga petechia). Behav Ecol Sociobiol 68:669–680

    Article  Google Scholar 

  • Harper D (1999) Feather mites, pectoral muscle condition, wing length, and plumage coloration of passerines. Anim Behav 58:553–562

    Article  PubMed  Google Scholar 

  • Hill G, Montgomerie R, Roeder C, Boag P (1994) Sexual selection and cuckoldry in a monogamous songbird: implications for sexual selection theory. Behav Ecol Sociobiol 35:193–199

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1006

    Article  PubMed  Google Scholar 

  • Kappes PJ, Stutchbury BJM, Woolfenden BE (2009) The relationship between carotenoid-based coloration and pairing, within- and extra-pair mating success in the American redstart. Condor 111:684–693

    Article  Google Scholar 

  • Kempenaers B (1997) Does breeding synchrony limit male opportunities or enhance female choice for extrapair paternity? Behaviour 134:551–562

    Article  Google Scholar 

  • Kempenaers B, Verheyen G, van den Broeck M, Burke T, van Broeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high quality males in the blue tit. Nature 357:494–496

    Article  Google Scholar 

  • Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Article  Google Scholar 

  • Kokko H, Morrell L (2005) Mate guarding, male attractiveness, and paternity under social monogamy. Behav Ecol 16:724–731

    Article  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2013) lmerTest: tests for random and fixed effect for linear mixed effect models (lmer objects of lme4 package). R package version 1.1-0. http://CRAN.R-project.org/package=lmerTest

  • LeBas N (2006) Female finery is not for males. Trends Ecol Evol 21:170–173

    Article  PubMed  Google Scholar 

  • Lifjeld J, Slagsvold T, Dale S, Ellegren H (1997) A sexually selected paradox in the pied flycatcher: attractive males are cuckolded. Auk 114:112–115

    Article  Google Scholar 

  • Longmire J, Maltbie M, Baker R (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Museum of Texas Tech University Occasional Papers 163, Lubbock

    Google Scholar 

  • McGraw K, Safran R, Evans M, Wakamatsu K (2004) European barn swallows use melanin pigments to color their feathers brown. Behav Ecol 15:889–891

    Article  Google Scholar 

  • Møller AP, Saino N, Taramino G, Galeotti P, Ferrario S (1998) Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the barn swallow. Am Nat 151:236–242

    Article  PubMed  Google Scholar 

  • Nordeide J, Kekalainen J, Janhunen M, Kortet R (2013) Female ornaments revisited—are they correlated with offspring quality? J Anim Ecol 82:26–38

    Article  PubMed  Google Scholar 

  • Øigarden T, Borge T, Lifjeld JT (2010) Extra-pair paternity and genetic diversity: the white-throated dipper Cinclus cinclus. J Avian Biol 41:248–257

    Article  Google Scholar 

  • Pilastro A, Griggio M, Matessi G (2003) Male rock sparrows adjust their breeding strategy according to female ornamentation: parental or mating investment? Anim Behav 66:265–271

    Article  Google Scholar 

  • Pryke S, Rollins L, Griffith S (2010) Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science 329:964–967

    Article  CAS  PubMed  Google Scholar 

  • Pyle P (1997) Identification guide to North American birds. Slate Creek Press, Bolinas

    Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

  • Safran R, McGraw K (2004) Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows. Behav Ecol 15:455–461

    Article  Google Scholar 

  • Safran R, Neuman C, McGraw K, Lovette I (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212

    Article  CAS  PubMed  Google Scholar 

  • Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  • Studd M, Robertson R (1985a) Evidence for reliable badges of status in territorial yellow warblers (Dendroica petechia). Anim Behav 33:1102–1113

    Article  Google Scholar 

  • Studd M, Robertson R (1985b) Sexual selection and variation in reproductive strategy in male yellow warblers (Dendroica petechia). Behav Ecol Sociobiol 17:101–109

    Google Scholar 

  • Studd M, Robertson R (1989) Influence of age and territory quality on the reproductive behaviour of male yellow warblers. Can J Zool 67:268–273

    Article  Google Scholar 

  • Taff CC, Steinberger D, Clark C, Belinsky K, Sacks H, Freeman-Gallant CR, Dunn PO, Whittingham LA (2012) Multimodal sexual selection in a warbler: plumage and song are related to different fitness components. Anim Behav 84:813–821

    Article  Google Scholar 

  • Thusius K, Peterson K, Dunn PO, Whittingham LA (2001) Male mask size is correlated with mating success in the common yellowthroat. Anim Behav 62:435–446

    Article  Google Scholar 

  • Tobias J, Montgomerie R, Lyon B (2013) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil Trans R Soc Lond B 367:2274–2293

    Article  Google Scholar 

  • Torres R, Velando A (2005) Male preference for female foot colour in a seabird with a mixed mating strategy. Anim Behav 69:59–65

  • Tuttle E (2003) Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence. Behav Ecol 14:425–432

    Article  Google Scholar 

  • Webster M, Pruett-Jones S, Westneat D, Arnold S (1995) Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49:1147–1157

    Article  Google Scholar 

  • Webster M, Chuang-Dobbs H, Holmes R (2001) Microsatellite identification of extrapair sires in a socially monogamous warbler. Behav Ecol 12:439–446

    Article  Google Scholar 

  • Webster M, Tarvin K, Tuttle E, Pruett-Jones S (2007) Promiscuity drives sexual selection in a socially monogamous bird. Evolution 61:2206–2211

    Article  Google Scholar 

  • Whittingham LA, Dunn PO (2005) Effects of extra-pair and within-pair reproductive success on the opportunity for selection in birds. Behav Ecol 16:138–144

    Article  Google Scholar 

  • Wouter F, van Dougen D, Mulder R (2009) Multiple ornamentation, female breeding synchrony, and extra-pair mating success of golden whistlers (Pachycephala pectoralis). J Ornithol 150:607–620

    Article  Google Scholar 

  • Yezerinac SM, Weatherhead PJ (1997) Extra-pair mating, male plumage coloration and sexual selection in yellow warblers (Dendroica petechia). Proc R Soc Lond B 264:527–532

    Article  Google Scholar 

  • Yezerinac SM, Weatherhead PJ, Boag P (1995) Extra-pair paternity and the opportunity for sexual selection in a socially monogamous bird (Dendroica petechia). Behav Ecol Sociobiol 37:179–188

    Article  Google Scholar 

  • Yezerinac SM, Weatherhead PJ, Boag P (1996) Cuckoldry and lack of parentage-dependent paternal care in yellow warblers: a cost–benefit approach. Anim Behav 52:821–832

    Article  Google Scholar 

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Acknowledgments

We thank the Sierra Nevada Aquatic Research Laboratory (SNARL) and the Inyo National Forest for providing facilities and access to field sites, with particular thanks to SNARL’s director, Daniel Dawson. Our sincere thanks to Bradley Hyman (University of California, Riverside) for allowing access to the genetic research equipment and supplies in his laboratory, and to Samantha Lewis for familiarizing the authors with genetic research procedures. John Rotenberry provided essential guidance when developing research plans and preparing the manuscript, and Stephen Myers sponsored the bird-banding sub-permit (United States Geological Survey) essential to this research. Thanks also to Marlene Zuk and Daphne Fairbairn for comments that aided in improving the manuscript. The University of California Natural Reserve System’s Mildred E. Mathias research grant, Sigma Xi, and the Valentine Eastern Sierra Reserve’s graduate student research grant provided funding.

Ethical standards and conflicts of interest

We conducted all field methods in accordance with rigorous ethical and legal standards, and the University of California, Riverside’s Institutional Animal Care and Use Committee approved all procedures. The authors declare that they have no conflict of interest.

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Correspondence to Andrea S. Grunst.

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Communicated by K. McGraw

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Grunst, A.S., Grunst, M.L. Multiple sexual pigments, assortative social pairing, and genetic paternity in the yellow warbler (Setophaga petechia). Behav Ecol Sociobiol 68, 1451–1463 (2014). https://doi.org/10.1007/s00265-014-1752-5

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