Multimodal flight display of a neotropical songbird predicts social pairing but not extrapair mating success
- 362 Downloads
Models of sexual selection predict that socially monogamous females may gain direct or indirect (genetic) benefits by mating with multiple males. We addressed current hypotheses by investigating how, in the socially monogamous blue-black grassquit (Volatinia jacarina), male courtship and territory quality varied with social and extrapair paternity. Males of this tropical granivorous passerine exhibit multimodal displays integrating motor (leap displays) and acoustic components. Across 3 years, we found that extrapair paternity ranged from 8 to 34 % of all nestlings and from 11 to 47 % of all broods. Extrapair and socially paired male territories had similar seed densities. Females preferred to pair socially with males executing higher leaps, but no other male display characteristic associated with paternity loss and extrapair fertilizations. Extrapair and social mates did not differ in genetic similarity to female partners nor in inbreeding levels. Additionally, inbreeding and body condition of extrapair and within-pair nestlings did not differ. Thus, not only did we reject the direct benefits hypothesis for extrapair copulations, but our results also did not support the additive and nonadditive genetic benefits hypotheses. Instead, we found support for benefits through selection of potentially “good fathers,” specifically for females that chose to pair socially with males exhibiting enhanced performance in their displays.
Multiple mating by females is intriguing because resulting advantages seem improbable. However, access to resources, genetic compatibility with the sexual partner and good gene transmission to the offspring are possible explanations for this behavior in several animals, including socially monogamous species. We investigated potential benefits in a socially monogamous neotropical bird, the blue-black grassquit. Males attract females using a sexual display of repeated leap flights synchronized with a song. We found that when selecting social mates, females favor higher-leaping males, an attribute associated with enhanced body condition that could indicate the capacity for better parenting and also be inherited by the offspring. Yet, when choosing extrapair males, females did not appear to base choices on leap parameters, vocal attributes, and genetic compatibility. These results do not suggest benefits for multiple mating by females, but show that selection of males in good physical condition can influence choice for social mates.
KeywordsGood genes Multimodal signals Polyandry Sexual selection Social monogamy
We thank all assistants that contributed to both fieldwork and video data processing, Tanya Sneddon for assistance in the Molecular Ecology Laboratory at University of St Andrews and two anonymous reviewers for suggestions that improved the manuscript.
Compliance with ethical standards
This study was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (AEX 4837/14-2), the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (471945/2013-7, GM/GD 142255/2012-2), the National Science Foundation (IOS-1028964), the Student Research Grant of the Animal Behavior Society, the University of St Andrews (UMGM7014), and the Universidade de Brasília. Logistic support was provided by Universidade de Brasília, University of Massachusetts - Amherst, and University of St. Andrews.
Conflict of interest
The authors declare that they have no conflict of interest.
All methods used in this study are in accordance with ethical standards and Brazilian laws and were approved by the relevant authorities: Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA (license no. 17765-1) and by the Centro Nacional de Pesquisas para Conservação das Aves Silvestres – CEMAVE (license no. 1301).
This article does not contain any studies with human participants performed by any of the authors.
- Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868Google Scholar
- Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New JerseyGoogle Scholar
- Bradbury JW, Vehrencamp SL (1998) Principles of animal communication, 2nd edn. Sinauer Associates, Sunderland, MAGoogle Scholar
- Brooks RC, Griffith SC (2010) Mate choice. In: Westneat DF, Fox CW (eds) Evolutionary behavioral ecology. Oxford University Press, Oxford, pp. 416–433Google Scholar
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, NYGoogle Scholar
- Dias A (2009) Comparação e descrição de parâmetros acústicos do canto de Volatinia jacarina (Aves: Emberizidae) no contexto da seleção sexual. Dissertation, Universidade de BrasíliaGoogle Scholar
- Dias RI, Macedo RH (2011) Nest predation versus resources in a Neotropical passerine: constraints of the food limitation hypothesis. Ornis Fenn 88:30–39Google Scholar
- Gowaty PA (1996) Battles of the sexes and origins of monogamy. In: Black JM (ed) Partnerships in birds: the study of monogamy. Oxford University Press, London, pp. 21–52Google Scholar
- Grunst AS, Grunst ML (2014) Multiple sexual pigments, assortative social pairing, and genetic paternity in the yellow warbler (Setophaga petechia). Behav Ecol Sociobiol:1451–1463Google Scholar
- Hsu Y-H, Schroeder J, Winney I, Burke T, Nakagawa S (2014) Costly infidelity: low lifetime fitness of extra-pair offspring in a passerine bird. Evolution, 2873–2884Google Scholar
- Johnstone RA (1997) The evolution of animal signals. In: Krebs JR, Davies NB (eds) Behavioural ecology, 4th edn. Blackwell Publishing, Oxford, pp. 155–178Google Scholar
- Manica LT, Podos J, Graves J, Macedo RH (2013) Flights of fancy: mating behavior, displays and ornamentation in a neotropical bird. In: Macedo R, Machado G (eds) Sexual selection. Perspectives and models from the Neotropics. Academic Press, San Diego, CA, pp. 391–407Google Scholar
- Manica LT, Macedo RH, Graves J, Podos J (2016) Vigor and skill in the acrobatic mating display of a neotropical songbird. Behav Ecol (in press)Google Scholar
- Mazerolle MJ (2010) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 1.25, https://www.r-project.org
- Møller AP, Pomiankowski A (1993) Why have birds got multiple sexual ornaments? Behav Ecol Sociobiol 32:167–176Google Scholar
- R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
- Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton, NJGoogle Scholar
- Sick H (2001) Ornitologia brasileira. Editora Nova Fronteira, Rio de Janeiro, RJGoogle Scholar
- Wagner RH (1998) Hidden leks: sexual selection and the clustering of avian territories. In: Parker P, Burley N (eds) Avian reproductive tactics: female and male perspectives. Ornithological Monographs. Allen Press, Lawrence, KS, pp. 123–145Google Scholar
- Winternitz JC, Promerova M, Polakova R, Vinker M, Schnitzer J, Munclinger P, Babik W, Radwan J, Bryja J, Albrecht T (2015) Effects of heterozygosity and MHC diversity on patterns of extra-pair paternity in the socially monogamous scarlet rosefinch. Behav Ecol Sociobiol 69:459–469CrossRefGoogle Scholar