Abstract
In many migratory songbirds, males arrive earlier at stopover sites and at the breeding grounds (‘protandry’) and older birds precede younger ones, but less is known about age differences in protandry. In seasonal environments, differential timing by sex and age is thought to reflect selection imposed by seasonality (i.e., viability selection) and intrasexual competition for space and mates. Viability and sexual selection can also favor male-biased sexual size dimorphism (SSD), leading to a positive relationship between protandry and SSD among species. We evaluated whether the relationship between protandry during spring migration and SSD in wing length (SSDW) differed between age classes in 20 sexually dimorphic songbirds. Consistent with the hypothesis that older, higher-quality males can better afford to arrive early, we found a stronger relationship between protandry and SSDW among older birds than among first-time breeders. We also tested the relationship between protandry and sexual size dimorphism of the wingtip (SSDWT) and found that greater age differences in protandry were related to greater age differences in SSDWT. We conclude that larger body sizes, energetically efficient wing shapes, and experience together select for the earlier arrival timing of older males relative to first-time breeding males and females.
Zusammenfassung
Der Zusammenhang zwischen Protandrie und Größendimorphismus beider Geschlechter ist bei Singvögeln altersspezifisch
Bei vielen Zugvögeln kommen die Männchen früher an den Rastplätzen und in den Brutgebieten an („Protandrie“), und die älteren Vögel kommen vor den jüngeren, aber über Altersunterschiede bei der Protandrie ist wenig bekannt. Für jahreszeitlich wechselnde Lebensräume wird angenommen, dass ein unterschiedliches Timing nach Alter und Geschlecht eine von der Jahreszeit abhängige Selektion (d.h. Selektion der Lebensfähigkeit) und einen innergeschlechtlichen Wettbewerb um Raum und Partner widerspiegelt. Lebensfähigkeit und sexuelle Selektion könnten auch einen die Männchen bevorzugenden Geschlechts-Größendimorphismus (SSD) begünstigen, was bei diesen Arten zu einem positiven Zusammenhang zwischen Protandrie und SSD führen würde. Wir untersuchten bei 20 geschlechtsdimorphen Singvögeln, ob sich der Zusammenhang zwischen Protandrie während des Frühjahrszuges und SSD in der Flügellänge (SSDW) zwischen den verschiedenen Altersklassen unterscheidet. Im Einklang mit der Hypothese, dass es sich ältere, qualitativ bessere Männchen eher leisten können, früher anzukommen, fanden wir bei älteren Vögeln einen stärkeren Zusammenhang zwischen Protandrie und SSDW als bei Erstbrütern. Wir untersuchten auch den Zusammenhang zwischen Protandrie und Geschlechts-Größendimorphismus bei den Flügelspitzen (SSDWT) und stellten fest, dass größere Altersunterschiede in der Protandrie mit größeren Altersunterschieden in der SSDWT zusammenhängen. Wir schließen daraus, dass alles zusammen—größere Körpergrößen, energetisch effiziente Flügelformen und Erfahrung—einer früheren Ankunft älterer Männchen im Vergleich zu erstmalig brütenden Männchen und Weibchen einen Selektionsvorteil bietet.
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Data availability
The Canadian Migration Monitoring Network data that support the findings of this study are available with permission from NatureCounts, a node of the Avian Knowledge Network, Birds Canada. [“http://www.naturecounts.ca”].
References
Arizaga J, Sánchez JM, Díez E et al (2011) Fuel load and potential flight ranges of passerine birds migrating through the western edge of the Pyrenees. Acta Ornithol 46:19–28
Bartoń K (2023) MuMIn: Multi-Model Inference. R package version 1.47.5. https://CRAN.R-project.org/package=MuMIn.
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bejarano V, Jahn AE (2018) Relationship between arrival timing and breeding success of intra-tropical migratory Fork-tailed Flycatchers (Tyrannus savana). J Field Ornithol 89:109–116
Blanckenhorn WU (2005) Behavioral causes and consequences of sexual size dimorphism. Ethology 111:977–1016
Bowlin MS (2007) Sex, wingtip shape, and wing-loading predict arrival date at a stopover site in the Swainson’s Thrush (Catharus ustulatus). Auk 124:1388–1396
Briedis M, Bauer S, Adamík P, Alves JA, Costa JS, Emmenegger T, Gustafsson L, Koleček J, Liechti F, Meier CM et al (2019) A full annual perspective on sex-biased migration timing in long-distance migratory birds. P R Soc b 286(1897):20182821
Colling O, Guglielmo C, Bonner S, Morbey Y (2022) Migratory songbirds and urban window collision mortality: vulnerability depends on species, diel timing of migration, and age class. Avian Conserv Ecol 17:22
Cooper NW, Murphy MT, Redmond LJ (2009) Age- and sex-dependent spring arrival dates of Eastern Kingbirds. J Field Ornithol 80:35–41
Cooper NW, Murphy MT, Redmond LJ, Dolan AC (2011) Reproductive correlates of spring arrival date in the Eastern Kingbird Tyrannus tyrannus. J Ornithol 152:143–152
Coppack T, Pulido F (2009) Proximate control and adaptive potential of protandrous migration in birds. Integr Comp Biol 49:493–506
Corvidae EL, Bierregaard RO, Peters SE (2006) Comparison of wing morphology in three birds of prey: Correlations with differences in flight behavior. J Morphol 267:612–622
Crysler ZJ, Ronconi RA, Taylor PD (2016) Differential fall migratory routes of adult and juvenile Ipswich Sparrows (Passerculus sandwichensis princeps). Mov Ecol 4:3
De la Hera I, Pulido F, Visser ME (2014) Longitudinal data reveal ontogenetic changes in the wing morphology of a long-distance migratory bird. Ibis 156:209–214
Fernández G, Lank DB, Sandercock BK (2007) Variation in the wing morphology of Western Sandpipers (Calidris mauri) in relation to sex, age class, and annual cycle. Auk 124:1037–1046
Fox J, Weisberg S (2018) An R companion to applied regression, 3rd edn. Thousand Oaks, CA
Francis CM, Cooke F (1986) Differential timing of spring migration in wood warblers (Parulinae). Auk 103:548–556
Guglielmo CG, Morbey YE, Kennedy LV, Deakin JE, Brown JM, Beauchamp AT (2022) A scaling approach to understand the dynamics of fat and lean mass in refueling migrant songbirds measured by quantitative magnetic resonance. Front Ecol Evol 10:787623
Hedenström A (2008) Adaptations to migration in birds: behavioural strategies, morphology, and scaling effects. Philos T R Soc B 363(1490):287–299
Hill GE (1989) Late spring arrival and dull nuptial plumage: aggression avoidance by yearling males? Anim Behav 37:665–673
Jetz W, Thomas GH, Joy JB, Redding DW, Hartmann K, Mooers AO (2014) Global distribution and conservation of evolutionary distinctness in birds. Curr Biol 24:919–930
Kahle D, Wickham H (2013) ggmap: Spatial Visualization with ggplot2. The R Journal 5: 144–161. http://journal.r-project.org/archive/2013-1/kahle-wickham.pdf
Kissner KJ, Weatherhead PJ, Francis CM (2003) Sexual size dimorphism and timing of spring migration in birds. J Evol Biol 16:154–162
Kokko H, Gunnarsson TG, Morrell LJ, Gill JA (2006) Why do female migratory birds arrive later than males? J Anim Ecol 75:1293–1303
Lenth RV (2023) emmeans: estimated marginal means, aka least-squares means. R package version 1.8.5. https://CRAN.R-project.org/package==emmeans.
Lockwood R, Swaddle JP, Rayner JMV (1998) Avian wingtip shape reconsidered: Wingtip shape indices and morphological adaptations to migration. J Avian Biol 29:273–292
Long Point Bird Observatory (2008) Canadian migration monitoring network—banding. Data accessed from NatureCounts, a node of the Avian Knowledge Network, Birds Canada. Available: http://www.naturecounts.ca/. Accessed <<August 2022>>.
Lozano GA, Perreault S, Lemon RE (1996) Age, arrival date and reproductive success of male American Redstarts Setophaga ruticilla. J Avian Biol 27:164–170
Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886
Matyjasiak P, López-Calderón C, Ambrosini R et al (2022) Wing morphology covaries with migration distance in a highly aerial insectivorous songbird. Curr Zool 44:5
McKinnon EA, Fraser KC, Stanley CQ, Stutchbury BJM (2014) Tracking from the tropics reveals behaviour of juvenile songbirds on their first spring migration. PLoS ONE 9:e105605
Mitchell GW, Woodworth BK, Taylor PD, Norris DR (2015) Automated telemetry reveals age specific differences in flight duration and speed are driven by wind conditions in a migratory songbird. Mov Ecol 3:19
Møller AP (1994) Phenotype-dependent arrival time and its consequences in a migratory bird. Behav Ecol Sociobiol 35:115–122
Morbey YE (2013) Protandry, sexual size dimorphism, and adaptive growth. J Theor Biol 338:93–99
Morbey YE, Hedenström A (2020) Leave earlier or travel faster? Optimal mechanisms for managing arrival time in migratory songbirds. Front Ecol Evol 7:492
Morbey YE, Ydenberg RC (2001) Protandrous arrival timing to breeding areas: a review. Ecol Lett 4:663–673
Morbey YE, Coppack T, Pulido F (2012) Adaptive hypotheses for protandry in arrival to breeding areas: a review of models and empirical tests. J Ornithol 153:207–215
Neate-Clegg MHC, Tingley MW (2023) Adult male birds advance spring migratory phenology faster than females and juveniles across North America. Glob Change Biol 29:341–354
Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N, Pearse W (2018) caper: Comparative analyses of Phylogenetics and Evolution in R. R package version 1.0.1. https://CRAN.R-project.org/package=caper.
Ouwehand J, Both C (2017) African departure rather than migration speed determines variation in spring arrival in Pied Flycatchers. J Anim Ecol 86:88–97
Ożarowska A, Zaniewicz G, Meissner W (2021) Sex and age-specific differences in wing pointedness and wing length in blackcaps Sylvia atricapilla migrating through the southern Baltic coast. Curr Zool 67:271–277
Paradis E, Schliep K (2019) ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528
Pedersen L, Jakobsen NM, Strandberg R et al (2019) Sex-specific difference in migration schedule as a precursor of protandry in a long-distance migratory bird. Sci Nat 106:45
Pyle P (1997) Identification guide to North American birds, Part 1. Slate Creek Press, Bolinas
R Core Team (2022) R: A language and environment for statistical computing. http://www.R-project.org/.
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223
Rubolini D, Spina F, Saino N (2004) Protandry and sexual dimorphism in trans-Saharan migratory birds. Behav Ecol 15:592–601
Rubolini D, Liker A, Garamszegi LZ et al (2015) Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: a primer. Curr Zool 61:959–965
Saino N, Rubolini D, Serra L, Caprioli M, Morganti M, Ambrosini R, Spina F (2010) Sex-related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry. J Evol Biol 23:2054–2065
Saino N, Rubolini D, Ambrosini R et al (2017) Sex- and age-dependent morphology and selection on wing shape in the Barn Swallow Hirundo rustica. J Avian Biol 48:1441–1450
Santos Baquero O (2019) ggsn: North Symbols and Scale Bars for Maps Created with ‘ggplot2’ or ‘ggmap’. R package version 0.5.0. https://CRAN.R-project.org/package=ggsn
Schmaljohann H, Meier C, Arlt D, Bairlein F, van Oosten H, Morbey YE, Åkesson S, Buchmann M, Chernetsov N, Desaever R et al (2016) Proximate causes of avian protandry differ between subspecies with contrasting migration challenges. Behav Ecol 27:321–331
Sergio F, Tanferna A, De Stephanis R, Jiménez LL, Blas J, Tavecchia G, Preatoni D, Hiraldo F (2014) Individual improvements and selective mortality shape lifelong migratory performance. Nature 515(7527):410–413
Smith RJ (1999) Statistics of sexual size dimorphism. J Hum Evol 36:423–458
Smith RJ, Moore FR (2005) Arrival timing and seasonal reproductive performance in a long-distance migratory landbird. Behav Ecol Sociobiol 57:231–239
Stewart RLM, Francis CM, Massey C (2002) Age-related differential timing of spring migration within sexes in passerines. Wilson Bull 114:264–271
Szász E, Jablonszky M, Krenhardt K, Markó G, Hegyi G, Herényi M, Laczi M, Nagy G, Rosivall B, Szöllősi E et al (2019) Male territorial aggression and fitness in Collared Flycatchers: a long-term study. Sci Nat 106:11
Tøttrup AP, Thorup K (2008) Sex-differentiated migration patterns, protandry and phenology in North European songbird populations. J Ornithol 149:161–167
Vágási CI, Pap PL, Vincze O, Osváth G, Erritzøe J, Møller AP (2016) Morphological adaptations to migration in birds. Evol Biol 43:48–59
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org
Wobker J, Heim W, Schmaljohann H (2021) Sex, age, molt strategy, and migration distance explain the phenology of songbirds at a stopover along the East Asian flyway. Behav Ecol Sociobiol 75:25
Woodworth BK, Newman AEM, Turbek SP, Dossman BC, Hobson KA, Wassenaar LI, Mitchell GW, Wheelwright NT, Norris DR (2016) Differential migration and the link between winter latitude, timing of migration, and breeding in a songbird. Oecologia 181:413–422
Acknowledgements
We thank Long Point Bird Observatory for supplying Canadian Migration Monitoring Network data, and all the volunteer participants who gathered data for the project. We are also thankful to Lauren Negrazis, Brittany Cooke, and David Burgess for help in the field, and D.J. Schramm for conducting the molecular sexing. Lastly, we would like to thank D. Rubolini and an anonymous reviewer for taking the time and effort to provide constructive feedback, valuable suggestions, and careful editing, which helped in improving the quality of the manuscript.
Funding
Funding contributions from Yolanda E. Morbey and Christopher G. Guglielmo were supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants. Contributions from Jessica E. Deakin were supported by a NSERC Postgraduate Scholarship—Doctoral.
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All authors worked to conceive and design this study. JED processed the banding data and conducted the statistical analyses with guidance from YEM. The first draft of the manuscript was written by JED and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Deakin, J.E., Guglielmo, C.G. & Morbey, Y.E. Covariation between protandry and sexual size dimorphism is age specific in songbirds. J Ornithol 165, 157–167 (2024). https://doi.org/10.1007/s10336-023-02082-8
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DOI: https://doi.org/10.1007/s10336-023-02082-8