Movement of the embryo is essential for musculoskeletal development in vertebrates, yet little is known about whether, and why, species vary. Avian brood parasites exhibit feats of strength in early life as adaptations to exploit the hosts that rear them. We hypothesized that an increase in embryonic movement could allow brood parasites to develop the required musculature for these demands. We measured embryo movement across incubation for multiple brood-parasitic and non-parasitic bird species. Using a phylogenetically controlled analysis, we found that brood parasites exhibited significantly increased muscular movement during incubation compared to non-parasites. This suggests that increased embryo movement may facilitate the development of the stronger musculoskeletal system required for the demanding tasks undertaken by young brood parasites.

American Museum of Natural History New York NY 10024 USA

c o Musumanene Farm PO Box 630038 Choma Zambia

Coucal Project PO Box 26 Chimala Tanzania

Department of Biological Sciences School of Life and Environmental Sciences Royal Holloway University of London Egham Surrey TW20 0EX UK

Department of Biology University of Dodoma PO Box 338 Dodoma Tanzania

Department of Evolution Ecology and Behavior School of Integrative Biology University of Illinois Urbana Champaign IL 61801 USA

Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK

FitzPatrick Institute of African Ornithology DST NRF Centre of Excellence University of Cape Town Rondebosch 7701 Cape Town South Africa

Max Planck Institut für Ornithologie Abteilung für Verhaltensneurobiologie Eberhard Gwinner Str 6a D 82319 Seewiesen Germany

The Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 603 65 Brno Czech Republic

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Müller GB. 2003. Embryonic motility: environmental influences and evolutionary innovation. Evol. Dev. 5, 56-60. (10.1046/j.1525-142X.2003.03009.x) PubMed DOI

Pitsillides AA. 2006. Early effects of embryonic movement: ‘a shot out of the dark.’ J. Anat. 208, 417-431. (10.1111/j.1469-7580.2006.00556.x) PubMed DOI PMC

Heywood JLL, McEntee GMM, Stickland NCC. 2005. In ovo neuromuscular stimulation alters the skeletal muscle phenotype of the chick. J. Muscle Res. Cell Motil. 26, 49-56. (10.1007/s10974-005-9007-8) PubMed DOI

Nowlan NC, Sharpe J, Roddy KA, Prendergast PJ, Murphy P. 2010. Mechanobiology of embryonic skeletal development: insights from animal models. Birth Defects Res. Part C Embryo Today Rev. 90, 203-213. (10.1002/bdrc.20184) PubMed DOI PMC

Hall BK, Herring SW. 1990. Paralysis and growth of the musculoskeletal system in the embryonic chick. J. Morphol. 206, 45-56. (10.1002/jmor.1052060105) PubMed DOI

Hosseini A, Hogg DA. 1991. The effects of paralysis on skeletal development in the chick embryo. II. Effects on histogenesis of the tibia. J. Anat. 177, 169-178. PubMed PMC

Felsenthal N, Zelzer E. 2017. Mechanical regulation of musculoskeletal system development. Development 144, 4271-4283. (10.1242/dev.151266) PubMed DOI PMC

Lemke SB, Schnorrer F. 2017. Mechanical forces during muscle development. Mech. Dev. 144, 92-101. (10.1016/j.mod.2016.11.003) PubMed DOI

Soler M. 2014. Long-term coevolution between avian brood parasites and their hosts. Biol. Rev. 89, 688-704. (10.1111/brv.12075) PubMed DOI

Stevens M. 2013. Bird brood parasitism. Curr. Biol. 23, 909-913. (10.1016/j.cub.2013.08.025) PubMed DOI

Davies NB, Nicholas B, Quinn D. 2000. Cuckoos, cowbirds and other cheats. London, UK: T & A D Poyser.

Igic B, Braganza K, Hyland MM, Silyn-Roberts H, Cassey P, Grim T, Rutila J, Moskát C, Hauber ME. 2011. Alternative mechanisms of increased eggshell hardness of avian brood parasites relative to host species. J. R. Soc. Interface 8, 1654-1664. (10.1098/rsif.2011.0207) PubMed DOI PMC

Rees JA, Cranston K. 2017. Automated assembly of a reference taxonomy for phylogenetic data synthesis. Biodivers. Data J. 5, 12581. (10.3897/BDJ.5.e12581) PubMed DOI PMC

Michonneau F, Brown JW, Winter DJ. 2016. ‘rotl’ : an R package to interact with the Open Tree of Life data. Methods Ecol. Evol. 7, 1476-1481. (10.1111/2041-210X.12593) DOI

Hauber ME, Moskát C. 2008. Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behav. Ecol. 19, 79-86. (10.1093/beheco/arm108) DOI

Kilner RM, Madden JR, Hauber ME. 2004. Broad parasitic cowbird nestlings use host young to procure resources. Science 305, 877-879. (10.1126/science.1098487) PubMed DOI

Lichtenstein G, Sealy SG. 1998. Nestling competition, rather than supernormal stimulus, explains the success of parasitic brown-headed cowbird chicks in yellow warbler nests. Proc. R. Soc. B 265, 249-254. (10.1098/rspb.1998.0289) DOI

Bortolato T, Gloag R, Reboreda JC, Fiorini VD. 2019. Size matters: shiny cowbirds secure more food than host nestmates thanks to their larger size, not signal exaggeration. Anim. Behav. 157, 201-207. (10.1016/j.anbehav.2019.09.009) DOI

Kilner RM. 2005. The evolution of virulence in brood parasites. Ornithol. Sci. 4, 55-64. (10.2326/osj.4.55) DOI

Honza M, Vošlajerová K, Moskát C. 2007. Eviction behaviour of the common cuckoo Cuculus canorus chicks. Commun. J. Avian Biol. 38, 385-389. (10.1111/j.2007.0908-8857.03901.x) DOI

Hauber ME. 2003. Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism. Behav. Ecol. 14, 227-235. (10.1093/beheco/14.2.227) DOI

Radin EL. 1986. Role of muscles in protecting athletes from injury. Acta Med. Scand. 220, 143-147. (10.1111/j.0954-6820.1986.tb08943.x) PubMed DOI

Suominen H. 2006. Muscle training for bone strength. Aging Clin. Exp. Res. 18, 85-93. (10.1007/BF03327422) PubMed DOI

Honza M, Feikusová K, Procházka P, Picman J. 2015. How to hatch from the common cuckoo (Cuculus canorus) egg: implications of strong eggshells for the hatching muscle (musculus complexus). J. Ornithol. 156, 679-685. (10.1007/s10336-015-1163-z) DOI

Antonov A, Stokke BG, Fossøy F, Liang W, Moksnes A, Røskaft E, Yang C, Møller AP. 2012. Why do brood parasitic birds lay strong-shelled eggs? Chinese Birds 3, 245-258. (10.5122/cbirds.2012.0039) DOI

Honza M, Picman J, Grim T, Novák V, Čapek M Jr, Mrlík V. 2001. How to hatch from an egg of great structural strength. A study of the common cuckoo. J. Avian Biol. 32, 249-255. (10.1111/j.0908-8857.2001.320307.x) DOI

Lipar JL, Ketterson ED. 2000. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc. R. Soc. B 267, 2005-2010. (10.1098/rspb.2000.1242) PubMed DOI PMC

Dearborn DC, MacDade LS, Robinson S, Dowling Fink AD, Fink ML. 2009. Offspring development mode and the evolution of brood parasitism. Behav. Ecol. 20, 517-524. (10.1093/beheco/arp026) DOI

Soler M, Soler JJ, Martínez JG, Moreno J. 1999. Begging behaviour and its energetic cost in great spotted cuckoo and magpie host chicks. Can. J. Zool. 77, 1794-1800. (10.1139/z99-128) DOI

Spottiswoode CN, Koorevaar J. 2012. A stab in the dark: chick killing by brood parasitic honeyguides. Biol. Lett. 8, 241-244. (10.1098/rsbl.2011.0739) PubMed DOI PMC

Spottiswoode CN, Stryjewski KF, Quader S, Colebrook-Robjent JFR, Sorenson MD. 2011. Ancient host specificity within a single species of brood parasitic bird. Proc. Natl Acad. Sci. USA 108, 17 738-17 742. (10.1073/pnas.1109630108) PubMed DOI PMC

Spottiswoode CN, Colebrook-Robjent JFRR. 2007. Egg puncturing by the brood parasitic greater honeyguide and potential host counteradaptations. Behav. Ecol. 18, 792-799. (10.1093/beheco/arm025) DOI

Short LL, Horne JFM. 2001. Toucans, barbets, and honeyguides: Ramphastidae, Capitonidae, and Indicatoridae. New York, NY: Oxford University Press.

Benz BW, Robbins MB, Peterson AT. 2006. Evolutionary history of woodpeckers and allies (Aves: Picidae): placing key taxa on the phylogenetic tree. Mol. Phylogenet. Evol. 40, 389-399. (10.1016/j.ympev.2006.02.021) PubMed DOI

Yang C, Huang Q, Wang L, Du WG, Liang W, Møller AP. 2018. Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs. Sci. Nat. 105, 10. (10.1007/s00114-017-1532-y) PubMed DOI

Gil D. 2003. Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50, 281-294.

Groothuis TGG, Schwabl H. 2008. Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil. Trans. R. Soc. B 363, 1647-1661. (10.1098/rstb.2007.0007) PubMed DOI PMC

Frésard L, Morisson M, Brun JM, Collin A, Pain B, Minvielle F, Pitel F. 2013. Epigenetics and phenotypic variability: some interesting insights from birds. Genet. Sel. Evol. 45, 1-12. (10.1186/1297-9686-45-16) PubMed DOI PMC

Payne RB. 2005. The cuckoos. Bird Families of the World. Oxford, UK: Oxford University Press.

Sorenson MD, Payne RB. 2002. Molecular genetic perspectives on avian brood parasitism. Integr. Comp. Biol. 42, 388-400. (10.1093/icb/42.2.388) PubMed DOI

McClelland SC, Jamie GA, Waters K, Caldas L, Spottiswoode CN, Portugal SJ. 2019. Convergent evolution of reduced eggshell conductance in avian brood parasites. Phil. Trans. R. Soc. B 374, 20180194. (10.1098/rstb.2018.0194) PubMed DOI PMC

Riehl C. 2016. Infanticide and within-clutch competition select for reproductive synchrony in a cooperative bird. Evolution 70, 1760-1769. (10.1111/evo.12993) PubMed DOI

Bryant DM, Tatner P. 1990. Hatching asynchrony, sibling competition and siblicide in nestling birds: studies of swiftlets and bee-eaters. Anim. Behav. 39, 657-671. (10.1016/S0003-3472(05)80377-X) DOI

Pollard AS, Pitsillides AA, Portugal SJ. 2016. Validating a noninvasive technique for monitoring embryo movement in ovo. Physiol. Biochem. Zool. 89, 331-339. (10.1086/687228) PubMed DOI

Angilletta MJ, Zelic MH, Adrian GJ, Hurliman AM, Smith CD. 2013. Heat tolerance during embryonic development has not diverged among populations of a widespread species (Sceloporus undulatus). Conserv. Physiol. 1, cot018. (10.1093/conphys/cot018) PubMed DOI PMC

Sheldon EL, McCowan LSC, McDiarmid CS, Griffith SC. 2018. Measuring the embryonic heart rate of wild birds: an opportunity to take the pulse on early development. Auk 135, 71-82. (10.1642/AUK-17-111.1) DOI

Colombelli-Négrel D, Hauber ME, Kleindorfer S. 2014. Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos. Proc. R. Soc. B 281, 20141154. (10.1098/rspb.2014.1154) PubMed DOI PMC

Murray JR, Varian-Ramos CW, Welch ZS, Saha MS. 2013. Embryological staging of the Zebra Finch, Taeniopygia guttata. J. Morphol. 274, 1090-1110. (10.1002/jmor.20165) PubMed DOI PMC

Lokemoen JT, Koford RR. 1996. Using candlers to determine the incubation stage of passerine eggs. J. F. Ornithol. 67, 660-668.

Hemmings N, Birkhead TR. 2016. Consistency of passerine embryo development and the use of embryonic staging in studies of hatching failure. Ibis (Lond. 1859) 158, 43-50. (10.1111/ibi.12336) DOI

Spottiswoode CN. 2013. A brood parasite selects for its own egg traits. Biol. Lett. 9, 20130573. (10.1098/rsbl.2013.0573) PubMed DOI PMC

Hoover JP, Hauber ME. 2007. Individual patterns of habitat and nest-site use by hosts promote transgenerational transmission of avian brood parasitism status. J. Anim. Ecol. 76, 1208-1214. (10.1111/j.1365-2656.2007.01291.x) PubMed DOI

Goymann W, Makomba M, Urasa F, Schwabl I. 2015. Social monogamy vs. polyandry: ecological factors associated with sex roles in two closely related birds within the same habitat. J. Evol. Biol. 28, 1335-1353. (10.1111/jeb.12657) PubMed DOI

Goymann W, Safari I, Muck C, Schwabl I.. 2016. Sex roles, parental care and offspring growth in two contrasting coucal species. R. Soc. Open Sci. 3, 160463. (10.1098/rsos.160463) PubMed DOI PMC

Portugal SJ, Ricketts RL, Chappell J, White CR, Shepard EL, Biro D. 2017. Boldness traits, not dominance, predict exploratory flight range and homing behaviour in homing pigeons. Phil. Trans. R. Soc. B 372, 20160234. (10.1098/rstb.2016.0234) PubMed DOI PMC

R Core Team. 2020. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See https://www.R-project.org/.

RStudio Team. 2020. RStudio: integrated development for R. Boston, MA: RStudio, PBC. See http://www.rstudio.com/.

White CR, Alton LA, Crispin TS, Halsey LG. 2016. Phylogenetic comparisons of pedestrian locomotion costs: confirmations and new insights. Ecol. Evol. 6, 6712-6720. (10.1002/ece3.2267) PubMed DOI PMC

Guigueno MF, Shoji A, Elliott KH, Aris-Brosou S. 2019. Flight costs in volant vertebrates: a phylogenetically-controlled meta-analysis of birds and bats. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 235, 193-201. (10.1016/j.cbpa.2019.06.003) PubMed DOI

Krüger O, Davies NB. 2002. The evolution of cuckoo parasitism: a comparative analysis. Proc. R. Soc. B 269, 375-381. (10.1098/rspb.2001.1887) PubMed DOI PMC

Sorenson MD, Payne RB. 2001. A single ancient origin of brood parasitism in African finches: implications for host–parasite coevolution. Evolution 55, 2550-2567. (10.1111/j.0014-3820.2001.tb00768.x) PubMed DOI

Garamszegi LZ. 2014. Modern phylogenetic comparative methods and their application in evolutionary biology, 1st edn. London, UK: Springer.

Covarrubias-Pazaran G. 2018. Software update: moving the R package sommer to multivariate mixed models for genome-assisted prediction. bioRxiv, 354639. (10.1101/354639) DOI

Hadfield JD, Nakagawa S. 2010. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494-508. (10.1111/j.1420-9101.2009.01915.x) PubMed DOI

Lenth R. 2020. emmeans: estimated marginal means, aka least-squares means. R package version 1.4.6.

Orme CDL, et al. 2006. Global patterns of geographic range size in birds. PLoS Biol. 4, 1276-1283. (10.1371/journal.pbio.0040208) PubMed DOI PMC

Kuznetsova A, Brockhoff PB, Christensen RHB. 2017. lmerTest package: tests in linear mixed effects models. J. Stat. Softw. 82, 1-26. (10.18637/jss.v082.i13) DOI

McClelland SC, et al. . 2021. Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies. Figshare. PubMed PMC

Highly virulent avian brood-parasitic species show elevated embryonic metabolic rates at specific incubation stages compared to less virulent and non-parasitic species

Parasitic fish embryos do a "front-flip" on the yolk to resist expulsion from the host

Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies

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