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Female ornamentation, incubation behavior, and reproductive success in a wild bird

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Abstract

In many species, both males and females possess sexual signals, but most research focuses on understanding signal expression in males. Females are often assumed to possess signals as a non-functional by-product of selection on males, but increasing evidence demonstrates functional explanations for variation in female signals. Theory suggests that—for many bird species—differences in long-term fitness associated with female signaling are more likely to be driven by variation in offspring quality than quantity, but research paradigms developed for studying male signals have primarily focused on counting offspring produced. Here, we tested the hypothesis that female ornamentation reliably signals the ability to incubate effectively. We used temperature loggers placed in the nest of common yellowthroat warblers (Geothlypis trichas) to record incubation behavior across multiple breeding attempts. Incubation bout length and the onset of daily activity were highly variable between females, but repeatable within females across multiple nesting attempts. Females with longer bouts and later onset of activity had higher hatching success. Wing length and plumage coloration were not related to incubation length or onset of activity, but were correlated with the total percentage of time spent on the nest each day. However, there was only a trend for repeatability in percentage of time spent on the nest and this measure was not correlated with any metrics of offspring quality or hatching success that we recorded. Therefore, we did not find any single aspect of incubation behavior that was (i) consistent, (ii) related to nestling quality or success, and (iii) signaled by ornamentation. Our results demonstrate the importance of variation in incubation behavior, but also suggest that ornaments are of limited utility as a signal of incubation ability in this species. Nevertheless, our study highlights the need to explore alternative fitness proxies in order to understand variation in female ornamentation.

Significance statement

Choosing a high-quality mate is an important determinant of reproductive success and animals often attend to elaborate ornaments as signals of quality during mate choice. In many species, both males and females have ornaments, but most research has focused on male signals and female mate choice. We found that female incubation behavior is associated with both plumage ornaments and hatching success, but there was no single signal that provided reliable information about the aspects of incubation behavior that were related to reproductive success. Our findings suggest that understanding female ornamentation may depend on considering the specific ways that females contribute to offspring survival.

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Data availability

All data and code required to produce the analyses and results presented here are archived online with Mendeley Data https://doi.org/10.17632/8mv667h87t.1.

References

  • Amundsen T (2000a) Female ornaments: genetically correlated or sexually selected. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic Press, Trondheim, Norway, pp 133–154

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Apakupakul K, Rubenstein DR (2015) Bateman’s principle is reversed in a cooperatively breeding bird. Biol Lett 11:20150034

    Article  PubMed  PubMed Central  Google Scholar 

  • Ardia D, Clotfelter E (2006) Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird. Behav Ecol 18:259–266

    Article  Google Scholar 

  • Ardia D, Pérez J, Chad E, Voss M, Clotfelter E (2009) Temperature and life history: experimental heating leads female tree swallows to modulate egg temperature and incubation behaviour. J Anim Ecol 78:4–13

    Article  PubMed  Google Scholar 

  • Ardia D, Pérez J, Clotfelter E (2010) Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proc R Soc Lond B 277:1881–1888

    Google Scholar 

  • Bartón K (2016) Mumin: multi-model inference. R package version 1.15.6, https://cran.R-project.Org/package=mumin

  • Bleu J, Agostini S, Biard C (2017) Nest-box temperature affects clutch size, incubation initiation, and nestling health in great tits. Behav Ecol 28:793–802

    Article  Google Scholar 

  • Coe BH, Beck ML, Chin SY, Jachowski CMB, Hopkins WA (2015) Local variation in weather conditions influences incubation behavior and temperature in a passerine bird. J Avian Biol 46:385–394

    Article  Google Scholar 

  • Cones AG, Liebl AL, Houslay TM, Russell AF (2020) Temperature-mediated plasticity in incubation schedules is unlikely to evolve to buffer embryos from climatic challenges in a seasonal songbird. J Evol Biol 34:465–476

    Article  PubMed  Google Scholar 

  • Conway CJ, Martin TE (2000a) Effects of ambient temperature on avian incubation behavior. Behav Ecol 11:178–188

    Article  Google Scholar 

  • Conway CJ, Martin TE (2000b) Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 54:670–685

    CAS  PubMed  Google Scholar 

  • Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M (2015) The effects of life history and sexual selection on male and female plumage colouration. Nature 527:367–370

    Article  CAS  PubMed  Google Scholar 

  • Doutrelant C, Gregoire A, Grnac N, Gomez D, Lambrechts M, Perret P (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233

    Article  CAS  PubMed  Google Scholar 

  • Dunn PO, Armenta JK, Whittingham LA (2015) Natural and sexual selection act on different axes of variation in avian plumage color. Sci Adv 1:e1400155

    Article  PubMed  PubMed Central  Google Scholar 

  • Fontaine JJ, Martin TE (2006) Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett 9:428–434

    Article  CAS  PubMed  Google Scholar 

  • Freeman-Gallant CR, Schneider RL, Taff CC, Dunn PO, Whittingham LA (2014) Contrasting patterns of selection on the size and coloration of a female plumage ornament in common yellowthroats. J Evol Biol 27:982–991

    Article  CAS  PubMed  Google Scholar 

  • Freeman-Gallant CR, Taff CC, Morin DF, Dunn PO, Whittingham LA, Tsang SM (2010) Sexual selection, multiple male ornaments, and age- and condition-dependent signaling in the common yellowthroat. Evolution 64:1007–1017

    Article  PubMed  Google Scholar 

  • Gerlach NM, McGlothlin JW, Parker PG, Ketterson ED (2012) Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species. Behav Ecol 23:1078–1088

    Article  Google Scholar 

  • Gorman H, Arnold K, Nager R (2005) Incubation effort in relation to male attractiveness in zebra finches (Taeniopygia guttata). J Avian Biol 36:413–420

    Article  Google Scholar 

  • Griffith S, Owens I, Thuman K (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  CAS  PubMed  Google Scholar 

  • Griggio M, Devigili A, Hoi H, Pilastro A (2009) Female ornamentation and directional male mate preference in the rock sparrow. Behav Ecol 20:1072–1078

    Article  Google Scholar 

  • Griggio M, Matessi G, Pilastro A (2003) Male Rock Sparrow (Petronia petronia) nest defence correlates with female ornament size. Ethology 109:659–669

    Article  Google Scholar 

  • Hasegawa M, Arai E (2016) Long incubation off-bouts of females paired with colorful males in barn swallows (hirundo rustica). Wilson J Ornithol 128:86–96

    Article  Google Scholar 

  • Hasegawa M, Arai E, Ito S, Wakamatsu K (2016) High brood patch temperature of less colourful, less pheomelanic female Barn Swallows Hirundo rustica. Ibis 156:808–820

    Article  Google Scholar 

  • Hasegawa M, Arai E, Watanabe M, Nakamura M (2012) High incubation investment of females paired to attractive males in barn swallows. Ornithol Sci 11:1–8

    Article  Google Scholar 

  • Kokko H (2017) Give one species the task to come up with a theory that spans them all: what good can come out of that? Proc R Soc B 284:20171652

    Article  PubMed  PubMed Central  Google Scholar 

  • Kokko H, Klug H, Jennions MD (2012) Unifying cornerstones of sexual selection: operational sex ratio, bateman gradient and the scope for competitive investment. Ecol Lett 15:1340–1351

    Article  PubMed  Google Scholar 

  • Kötél D, Laczi M, Török J, Hegyi G (2016) Mutual ornamentation and the parental behaviour of male and female Collared Flycatchers Ficedula albicollis during incubation. Ibis 158:796–807

    Article  Google Scholar 

  • Kraaijeveld K (2014) Reversible trait loss: the genetic architecture of female ornaments. Annu Rev Ecol Evol S 45:159–177

    Article  Google Scholar 

  • LaManna JA, Martin TE (2016) Costs of fear: behavioural and life-history responses to risk and their demographic consequences vary across species. Ecol Lett 19:403–413

    Article  PubMed  Google Scholar 

  • Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 292–305

  • López-Idiáquez D, Vergara P, Fargallo JA, Martínez-Padilla J (2016) Female plumage coloration signals status to conspecifics. Anim Behav 121:101–106

    Article  Google Scholar 

  • Mahr K, Griggio M, Granatiero M, Hoi H (2012) Female attractiveness affects paternal investment: experimental evidence for male differential allocation in blue tits. Front Zool 9:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin TE (2015) Age-related mortality explains life history strategies of tropical and temperate songbirds. Science 349:966–970

    Article  CAS  PubMed  Google Scholar 

  • Martin TE, Arriero E, Majewska A (2011) A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature. Bio Lett 7:425–428

    Article  Google Scholar 

  • Martin TE, Auer SK, Bassar RD, Niklison AM, Lloyd P (2007) Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569

    Article  PubMed  Google Scholar 

  • Martin TE, Schwabl H (2008) Variation in maternal effects and embryonic development rates among passerine species. Phil Trans R Soc B 363:1663–1674

    Article  PubMed  Google Scholar 

  • Martin TE, Ton R, Oteyza JC (2018) Adaptive influence of extrinsic and intrinsic factors on variation of incubation periods among tropical and temperate passerines. Auk 135:101–113

    Article  Google Scholar 

  • Matysioková B, Remeš V (2010) Incubation feeding and nest attentiveness in a social monogamous songbird: role of feather colouration, territory quality and ambient environment. Ethology 116:596–607

    Google Scholar 

  • Nakagawa S, Schielzeth H (2011) Repeatability for gaussian and non gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    Google Scholar 

  • Nakagawa S, Schielzeth H, O’Hara RB (2013) A general and simple method for obtaining r2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Nord A, Nilsson JÅ (2011) Incubation temperature affects growth and energy metabolism in blue tit nestlings. Am Nat 178:639–651

    Article  PubMed  Google Scholar 

  • Nordeide JT, Kekäläinen 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 

  • Odom KJ, Hall ML, Riebel K, Omland KE, Langmore NE (2014) Female song is widespread and ancestral in songbirds. Nat Commun 5:3379

    Article  PubMed  Google Scholar 

  • Palacios MG, Martin TE (2006) Incubation period and immune function: a comparative field study among coexisting birds. Oecologia 146:505–512

    Article  PubMed  Google Scholar 

  • Pearse AT, Cavitt JF, Cully JF (2004) Effects of food supplementation on female nest attentiveness and incubation mate feeding in two sympatric wren species. Wilson Bull 116:23–30

    Article  Google Scholar 

  • Pérez J, Ardia D, Chad E, Clotfelter E (2008) Experimental heating reveals nest temperature affects nestling condition in tree swallows (Tachycineta bicolor). Biol Lett 4:468–471

    Article  PubMed  PubMed Central  Google Scholar 

  • Plaza M, Cantarero A, Cuervo JJ, Moreno J (2018) Female incubation attendance and nest vigilance reflect social signaling capacity: a field experiment. Behav Ecol Sociobiol 72:24

    Article  Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org

  • Rosvall KA (2011) Intrasexual competition in females: evidence for sexual selection? Behav Ecol 22:1131–1140

    Article  PubMed  PubMed Central  Google Scholar 

  • Sæther BE (1989) Survival rates in relation to body weight in european birds. Ornis Scand 20:13–21

    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 

  • Stoffel MA, Nakagawa S, Schielzeth H (2017) Rptr: repeatability estimation and variance decomposition by generalized linear mixed-effects models. Methods Ecol Evol 8:1639–1644

    Article  Google Scholar 

  • Sullivan K (1989) Predation and starvation: age-specific mortality in juvenile juncos (Junco phaenotus). J Anim Ecol 58:275–286

    Article  Google Scholar 

  • Taff CC, Freeman-Gallant C, Dunn PO, Whittingham LA (2013) Spatial distribution of nests constrains the strength of sexual selection in a warbler. J Evol Biol 26:1392–1405

    Article  CAS  PubMed  Google Scholar 

  • Taff CC, Patricelli GL, Freeman-Gallant CR (2014) Fluctuations in neighbourhood fertility generate variable signalling effort. Proc R Soc B 281:20141974

    Article  PubMed  PubMed Central  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine Publishing Company, Chicago, pp 136–184

    Google Scholar 

  • Uehling J, Taff CC, Winkler D, Vitousek MN (2020) Developmental temperature predicts the adult response to stressors in a free-living passerine. J Anim Ecol 89:842–854

    Article  PubMed  Google Scholar 

  • Visser ME, Lessells CM (2001) The costs of egg production and incubation in great tits (Parus major). Proc R Soc Lond B 268:1271–1277

    Article  CAS  Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol S 34:365–396

    Article  Google Scholar 

  • Whittingham LA, Freeman-Gallant CR, Taff CC, Dunn PO (2015) Different ornaments signal male health and MHC variation in two populations of a warbler. Mol Ecol 24:1584–1595

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank L. Duval, E. Krasner, K. Littrell, and B. Massey for assistance collecting data in the field. We also thank the two anonymous reviewers and editors who provided helpful comments on the manuscript.

Funding

This work was financially supported by an NSF Graduate Research Fellowship, NSF Doctoral Dissertation Improvement Grant, and the Francine A. Bradley Award to CCT.

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Correspondence to Conor C. Taff.

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All applicable state, national, and institutional guidelines for the care and use of animals were followed. Research was conducted under UC Davis Institutional Animal Care and Use Committee protocol #16362 and Skidmore College IACUC protocol #69. Permission to capture and sample animals was granted by New York State (#1513) and federal (#10582) permits to CFG for this work.

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Communicated by Andrea Pilastro.

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Taff, C.C., Freeman-Gallant, C.R. Female ornamentation, incubation behavior, and reproductive success in a wild bird. Behav Ecol Sociobiol 75, 92 (2021). https://doi.org/10.1007/s00265-021-03033-0

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