Skip to main content
Log in

Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Evaluating the contribution of individual and environmental determinants of reproductive success is essential to improve our understanding of sexual selection. In socially monogamous bird species with high rates of extrapair paternity, traits or environmental contexts affecting the number of within-pair young (WPY) produced by males can differ from those affecting the number of extrapair young fathered (EPY). Here, we use a 4-year dataset collected in contrasted environments to assess the factors affecting male reproductive success in tree swallows (Tachycineta bicolor), a species showing high levels of extrapair paternity. Our analyses revealed that the number of WPY was higher under better environmental conditions, while the number of EPY was mainly related to male characteristics. Males nesting in more intensive agricultural areas had fewer WPY produced and a lower reproductive success. Also, males breeding earlier in the season had more WPY. The presence of parasites reduced males’ reproductive success, mainly by reducing the number of EPY. The influence of male phenotype varied according to population density: Tarsus length variation had a greater effect on reproductive success at low population density than at high density, while wing length was also positively related to the number of EPY, more so at high than at low density. Altogether, our results suggest a complex interplay between individual and environmental determinants of reproductive success and imply that sexual selection dynamics varies depending on environmental contexts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868

    Google Scholar 

  • Åkesson M, Bensch S, Hasselquist D (2007) Genetic and phenotypic associations in morphological traits: a long term study of great reed warblers Acrocephalus arundinaceus. J Avian Biol 38:58–72

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton, NJ, USA

    Google Scholar 

  • Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: theory. Evolution 38:709–719

    Article  Google Scholar 

  • Baeta R, Bélisle M, Garant D (2012a) Importance of breeding season and maternal investment in studies of sex-ratio adjustment: a case study using tree swallows. Biol Lett 8:401–404

    Article  PubMed Central  PubMed  Google Scholar 

  • Baeta R, Bélisle M, Garant D (2012b) Agricultural intensification exacerbates female-biased primary brood sex-ratio in tree swallows. Landscape Ecol 27:1395–1405

    Article  Google Scholar 

  • Barber CA, Robertson RJ, Boag PT (1996) The high frequency of extra-pair paternity in tree swallows is not an artifact of nestboxes. Behav Ecol Sociobiol 38:425–430

    Article  Google Scholar 

  • Barbosa A, Merino S, De Lope F, Møller AP (2002) Effects of feather lice on flight behavior of male barn swallows (Hirundo rustica). Auk 119:213–216

    Article  Google Scholar 

  • Barbraud C, Weimerskirch H (2005) Environmental conditions and breeding experience affect costs of reproduction in Blue Petrels. Ecology 86:682–692

    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

  • Birkhead TR, Møller AP (eds) (1998) Sperm competition and sexual selection. Academic Press, London

  • Bitton P-P, O'Brien EL, Dawson RD (2007) Plumage brightness and age predict extrapair fertilization success of male tree swallows, Tachycineta bicolor. Anim Behav 74:1777–1784

    Google Scholar 

  • Brown CR, Brown MB, Rannala B (1995) Ectoparasites reduce long-term survival of their avian host. Proc R Soc Lond B 262:313–319

    Google Scholar 

  • Canadian Wildlife Service (2004) Occupation du sol à partir des images classifiées Landsat-7, Sud du Québec, 1999–2003. Environnement Canada, région du Québec, Québec, Canada

  • Canal D, Potti J, Dávila JA (2011) Male phenotype predicts extra-pair paternity in pied flycatchers. Behaviour 148:691–712

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cleasby IR, Nakagawa S (2012) The influence of male age on within-pair and extra-pair paternity in passerines. Ibis 154:318–324

    Article  Google Scholar 

  • Clutton-Brock T, Sheldon BC (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends Ecol Evol 25:562–573

    Article  PubMed  Google Scholar 

  • Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10:248–252

    Article  PubMed  CAS  Google Scholar 

  • Conrad KF, Johnston PV, Crossman C, Kempenaers B, Robertson RJ, Wheelwright NT, Boag PT (2001) High levels of extra-pair paternity in an isolated, low-density, island population of tree swallows (Tachycineta bicolor). Mol Ecol 10:1301–1308

    Article  PubMed  CAS  Google Scholar 

  • Costantini D, Møller AP (2009) Does immune response cause oxidative stress in birds? A meta-analysis. Comp Biochem Physiol 153:339–344

    Article  CAS  Google Scholar 

  • Crawley MJ (2007) The R Book. Wiley, West Sussex

    Book  Google Scholar 

  • Crowe SA, Kleven O, Delmore KE, Laskemoen T, Nocera JJ, Lifjeld JT, Robertson RJ (2009) Paternity assurance through frequent copulations in a wild passerine with intense sperm competition. Anim Behav 77:183–187

    Article  Google Scholar 

  • Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45:173–180

    Article  PubMed  CAS  Google Scholar 

  • Di Giulio M, Edwards PJ, Meister E (2001) Enhancing insect diversity in agricultural grasslands: the roles of management and landscape structure. J Appl Ecol 38:310–319

    Article  Google Scholar 

  • Dunn PO, Whittingham LA (2005) Radio-tracking of female Tree Swallows prior to egg-laying. J Field Ornithol 76:259–263

    Google Scholar 

  • Dunn PO, Whittingham LA (2007) Search costs influence the spatial distribution, but not the level, of extra-pair mating in tree swallows. Behav Ecol Sociobiol 61:449–454

    Article  Google Scholar 

  • Dunn PO, Robertson RJ, Michaud-Freeman D, Boag PT (1994a) Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35:273–281

    Article  Google Scholar 

  • Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT (1994b) Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows. Behav Ecol 5:123–129

    Article  Google Scholar 

  • Dyrcz A, Wink M, Kruszewicz A, Leisler B (2005) Male reproductive success is correlated with blood parasite levels and body condition in the promiscuous aquatic warbler (Acrocephalus paludicola). Auk 122:558–565

    Article  Google Scholar 

  • Forbes MRL (1993) Parasitism and host reproductive effort. Oikos 67:444–450

    Article  Google Scholar 

  • Forsman AM, Vogel LA, Sakaluk SK, Johnson BG, Masters BS, Johnson LS, Thompson CF (2008) Female house wrens (Troglodytes aedon) increase the size, but not immunocompetence, of their offspring through extra-pair mating. Mol Ecol 17:3697–3706

    Article  PubMed  Google Scholar 

  • Fridolfsson A, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121

    Article  Google Scholar 

  • Garant D, Kruuk LEB, McCleery RH, Sheldon BC (2007) The effects of environmental heterogeneity on multivariate selection on reproductive traits in female great tits. Evolution 61:1546–1559

    Article  PubMed  Google Scholar 

  • Ghilain A, Bélisle M (2008) Breeding success of tree swallows along a gradient of agricultural intensification. Ecol Appl 18:1140–1154

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64

    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 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kempenaers B, Congdon B, Boag P, Robertson RJ (1999) Extrapair paternity and egg hatchability in tree swallows: evidence for the genetic compatibility hypothesis? Behav Ecol 10:304–311

    Article  Google Scholar 

  • Kempenaers B, Everding S, Bishop C, Boag P, Robertson RJ (2001) Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 49:251–259

    Article  Google Scholar 

  • Kose M, Møller AP (1999) Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45:430–436

    Article  Google Scholar 

  • Leffelaar D, Robertson RJ (1984) Do male tree swallows guard their mates? Behav Ecol Sociobiol 16:73–79

    Article  Google Scholar 

  • Lehtonen PK, Primmer CR, Laaksonen T (2009) Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca. Anim Behav 77:1103–1110

    Article  Google Scholar 

  • Lifjeld JT, Robertson RJ (1992) Female control of extra-pair fertilization in tree swallows. Behav Ecol Sociobiol 31:89–96

    Article  Google Scholar 

  • Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229

    Article  Google Scholar 

  • Mayer C, Pasinelli G (2013) New support for an old hypothesis: density affects extra-pair paternity. Ecol Evol 3:694–705

    Google Scholar 

  • Møller AP (1990a) Effects of parasitism by a haematophagous mite on reproduction in the barn swallow. Ecology 71:2345–2357

    Article  Google Scholar 

  • Møller AP (1990b) Parasites and sexual selection: current status of the Hamilton and Zuk hypothesis. J Evol Biol 3:319–328

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Paquette SR, Garant D, Pelletier F, Bélisle M (2013) Seasonal patterns in tree swallow prey (Diptera) abundance are affected by agricultural intensification. Ecol Appl 23:122–133

    Article  PubMed  Google Scholar 

  • Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–57

    Article  PubMed  CAS  Google Scholar 

  • Porlier M, Bélisle M, Garant D (2009) Non-random distribution of individual genetic diversity along an environmental gradient. Philos T Roy Soc B 364:1543–1554

    Google Scholar 

  • Porlier M, Charmantier A, Bourgault P, Perret P, Blondel J, Garant D (2012) Variation in phenotypic plasticity and selection patterns in blue tit breeding time: between- and within-population comparisons. J Anim Ecol 81:1041–1051

    Article  PubMed  Google Scholar 

  • Proctor H, Owens I (2000) Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15:358–364

    Article  PubMed  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/

  • Robinson MR, Sander van Doorn G, Gustafsson L, Qvarnström A (2012) Environment-dependent selection on mate choice in a natural population of birds. Ecol Lett 15:611–618

    Article  PubMed  Google Scholar 

  • Ryder TB, Fleischer RC, Shriver WG, Marra PP (2012) The ecological–evolutionary interplay: density-dependent sexual selection in a migratory songbird. Ecol Evol 2:976–987

    Article  PubMed Central  PubMed  Google Scholar 

  • Saino N, Primmer CR, Ellegren H, Møller AP (1999) Breeding synchrony and paternity in the barn swallow (Hirundo rustica). Behav Ecol Sociobiol 45:211–218

    Article  Google Scholar 

  • Sheldon BC, Kruuk LEB, Merilä J (2003) Natural selection and inheritance of breeding time and clutch size in the collared flycatcher. Evolution 57:406–420

    Article  PubMed  CAS  Google Scholar 

  • Stutchbury BJ, Morton ES (1995) The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132:675–690

    Article  Google Scholar 

  • Stutchbury BJ, Robertson RJ (1988) Within-season and age-related patterns of reproductive performance in female tree swallows (Tachycineta bicolor). Can J Zool 66:827–834

    Article  Google Scholar 

  • Teplitsky C, Mouawad NG, Balbontin J, De Lope F, Møller AP (2011) Quantitative genetics of migration syndromes: a study of two barn swallow populations. J Evol Biol 24:2025–2039

    Article  PubMed  CAS  Google Scholar 

  • Thusius KJ, Dunn PO, Peterson KA, Whittingham LA (2001) Extrapair paternity is influenced by breeding synchrony and density in the common yellowthroat. Behav Ecol 12:633–639

    Article  Google Scholar 

  • Weatherhead PJ, Boag PT (1995) Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91

    Article  Google Scholar 

  • Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215

    Article  Google Scholar 

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

    Google Scholar 

  • Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15:841–849

    Article  PubMed  Google Scholar 

  • Wiggins DA (1989) Heritability of body size in cross-fostered tree swallow broods. Evolution 43:1808–1811

    Article  Google Scholar 

  • Winkler DW, Hallinger KK, Ardia DR, Robertson RJ, Stutchbury BJ, Cohen RR (2011) Tree swallow (Tachycineta bicolor). The Birds of North America Online. http://bna.birds.cornell.edu/bna/. Accessed 01 Oct 2013

Download references

Acknowledgments

We thank the 40 farm owners who provided access to their lands. We also wish to thank all graduate students and field and laboratory assistants who have contributed in gathering data in our system over the years. We also thank Melissa Hughes and two anonymous reviewers for the comments on a previous version of this manuscript. This work was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) discovery grants to D.G., M.B., and F.P., by a strategic project research grant to D.G. and M.B. and by the Canada Research Chair program to F.P. and M.B.. A.B. was supported by a postgraduate NSERC scholarship.

Ethical standards

Animals were captured and handled in compliance with the Canadian Council on Animal Care, under the approval of the Université de Sherbrooke Animal Ethics Committee (protocol number: DG2010-01-Université de Sherbrooke).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dany Garant.

Additional information

Communicated by M. Hughes

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 325 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lessard, A., Bourret, A., Bélisle, M. et al. Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 68, 733–742 (2014). https://doi.org/10.1007/s00265-014-1686-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-014-1686-y

Keywords

Navigation