Highly virulent avian brood-parasitic species show elevated embryonic metabolic rates at specific incubation stages compared to less virulent and non-parasitic species
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
U54 MD017979
NIMHD NIH HHS - United States
Leverhulme Trust
Natural Environment Research Council
PubMed
39317329
PubMed Central
PMC11421897
DOI
10.1098/rsbl.2024.0411
Knihovny.cz E-zdroje
- Klíčová slova
- brood parasitism, cowbirds, cuckoos, embryo metabolism, honeyguides, respirometry,
- MeSH
- embryo nesavčí metabolismus MeSH
- energetický metabolismus MeSH
- hnízdění MeSH
- interakce hostitele a parazita * MeSH
- ptáci * parazitologie embryologie MeSH
- virulence MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
As the avian embryo grows and develops within the egg, its metabolic rate gradually increases. Obligate avian brood-parasitic birds lay their eggs in the nests of other species to avoid the costs of parental care, and all but one of these brood-parasitic species are altricial at hatching. Yet the chicks of some altricial brood-parasitic species perform the physically demanding task of evicting, stabbing or otherwise killing host progeny within days of hatching. This implies a need for high metabolic rates in the embryo, just as precocial species require. Using flow-through respirometry in situ, we investigated embryonic metabolic rates in diverse avian brood parasite lineages which either kill host offspring (high virulence) or share the nest with host young (low virulence). High-virulence brood parasite embryos exhibited higher overall metabolic rates than both non-parasitic (parental) species and low-virulence parasites. This was driven by significantly elevated metabolic rates around the halfway point of incubation. Additionally, a fine-scale analysis of the embryos of a host-parasitic pair showed faster increases in metabolic rates in the parasite. Together these results suggest that the metabolic patterns of the embryos of high-virulence parasites facilitate their early-life demands.
American Museum of Natural History New York NY 10024 USA
Auckland University of Technology Auckland 1010 New Zealand
c o Musumanene Farm Choma Zambia
Department of Biology The University of Oxford Oxford OX1 3SZ UK
Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK
School of Biological Sciences Monash University Clayton Victoria 3800 Australia
The Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 Brno 603 65 Czech Republic
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Croston R, Hauber ME.. 2010. The ecology of avian brood parasitism. Nat. Educ. Knowl. 1, 3.
Manna TJ, Hauber ME. 2016. Recognition, speciation, and conservation: recent progress in brood parasitism research among social insects. Curr. Opin. Behav. Sci. 12 , 1–5. (10.1016/j.cobeha.2016.07.005) DOI
Sato T. 1986. A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323 , 58–59. (10.1038/323058a0) PubMed DOI
Pollock HS, Hoover JP, Uy FMK, Hauber ME. 2021. Brood parasites are a heterogeneous and functionally distinct class of natural enemies. Tren. Paras. 37 , 588–596. (10.1016/j.pt.2021.02.005) PubMed DOI
Davies NB. 2000. Cuckoos, cowbirds and other cheats. London, UK: T & AD Poyser Ltd.
Grim T, Rutila J, Cassey P, Hauber ME. 2009. The cost of virulence: an experimental study of egg eviction by brood parasitic chicks. Behav. Ecol. 20 , 1138–1146. (10.1093/beheco/arp108) DOI
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
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
Rutila J, Latja R, Koskela K. 2002. The common cuckoo Cuculus canorus and its cavity nesting host, the redstart Phoenicurus phoenicurus: a peculiar cuckoo–host system? J. Avian Biol. 33 , 414–419. (10.1034/j.1600-048X.2002.02937.x) DOI
Antonson ND, Schelsky WM, Tolman D, Kilner RM, Hauber ME. 2022. Niche construction through a Goldilocks principle maximizes fitness for a nest-sharing brood parasite. Proc. R Soc. B 289 , 20221223. (10.1098/rspb.2022.1223) PubMed DOI PMC
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
Birkhead TR, Hemmings N, Spottiswoode CN, Mikulica O, Moskát C, Bán M, Schulze-Hagen K. 2011. Internal incubation and early hatching in brood parasitic birds. Proc. R. Soc. B 278 , 1019–1024. (10.1098/rspb.2010.1504) PubMed DOI PMC
Payne RB. 1977. The ecology of brood parasitism in birds. Annu. Rev. Ecol. Syst. 8 , 1–28. (10.1146/annurev.es.08.110177.000245) DOI
Török J, Moskát C, Michl G, Péczely P. 2004. Common cuckoos (Cuculus canorus) lay eggs with larger yolk but not more testosterone than their great reed warbler (Acrocephalus arundinaceus) hosts. Ethol. Ecol. Evol. 16 , 271–277. (10.1080/08927014.2004.9522638) DOI
Igic B, et al. . 2015. A nanostructural basis for gloss of avian eggshells. J. R. Soc. Interface 12 , 20141210. (10.1098/rsif.2014.1210) PubMed DOI PMC
Portugal SJ, Hauber ME, Maurer G, Stokke BG, Grim T, Cassey P. 2014. Rapid development of brood‐parasitic cuckoo embryos cannot be explained by increased gas exchange through the eggshell. J. Zool. 293 , 219–226. (10.1111/jzo.12144) DOI
Attard MRG, Portugal SJ. 2021. Climate variability and parent nesting strategies influence gas exchange across avian eggshells. Proc. R. Soc. B 288 , 20210823. (10.1098/rspb.2021.0823) PubMed DOI PMC
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
McClelland SC, Attard MRG, Bowen J, Horrocks NPC, Jamie GA, Dixit T, Spottiswoode CN, Portugal SJ. 2023. Eggshell composition and surface properties of avian brood-parasitic species compared with non-parasitic species. R. Soc. Open Sci. 10 , 221023. (10.1098/rsos.221023) PubMed DOI PMC
McClelland SC, et al. . 2021. Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies. Proc. R. Soc. B 288 , 20211137. (10.1098/rspb.2021.1137) PubMed DOI PMC
Vleck CM, Vleck D. 1996. Embryonic energetics. In Avian energetics and nutritional ecology, pp. 417–454. New York, NY: Chapman & Hall. (10.1007/978-1-4613-0425-8_12) DOI
Boersma PD. 1982. Why some birds take so long to hatch. Am. Nat. 120 , 733–750. (10.1086/284027) DOI
Vleck CM, Hoyt DF, Vleck D. 1979. Metabolism of avian embryos: patterns in altricial and precocialbirds. Physiol. Zool. 52 , 363–377. (10.1086/physzool.52.3.30155757) DOI
Vleck CM, Vleck D.. 1987. Metabolism and energetics of avian embryos. J. Exp. Zool. 1, 111–125. PubMed
Ricklefs RE. 1979. Patterns of growth in birds. a comparative study of development in the starling, common tern and Japanese quail. Auk 1 , 10–30. (10.1093/auk/96.1.10) DOI
Kilner RM. 2005. The evolution of virulence in brood parasites. Ornithol. Sci. 4 , 55–64. (10.2326/osj.4.55) DOI
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
Thorogood R, Spottiswoode CN, Portugal SJ, Gloag R. 2019. The coevolutionary biology of brood parasitism: a call for integration. Phil. Trans. R. Soc. B 374 , 20180190. (10.1098/rstb.2018.0190) PubMed DOI PMC
Goodchild CG, Grisham K, Belden JB, DuRant SE. 2020. Effects of sublethal application of deepwater horizon oil to bird eggs on embryonic heart and metabolic rate. Conserv. Biol. 34 , 1262–1270. (10.1111/cobi.13539) PubMed DOI
Mortola JP, Wills K, Trippenbach T, Al Awam K. 2010. Interactive effects of temperature and hypoxia on heart rate and oxygen consumption of the 3-day old chicken embryo. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 155 , 301–308. (10.1016/j.cbpa.2009.11.003) PubMed DOI
Ton R, Martin TE. 2017. Proximate effects of temperature versus evolved intrinsic constraints for embryonic development times among temperate and tropical songbirds. Sci. Rep. 7 , 895. (10.1038/s41598-017-00885-3) 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/.
R Studio Team . 2020. RStudio: Integrated Development for R. Boston, MA: RStudio, PBC. See http://www.rstudio.com/.
Baggot JD. 1978. Some aspects of clinical pharmacokinetics in veterinary medicine II. J. Vet. Pharmacol. Ther. 1 , 111–118. (10.1111/j.1365-2885.1978.tb00314.x) DOI
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
Pagel M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48 , 612–622. (10.1080/106351599260184) 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
Vanderweele TJ. 2010. Sufficient cause interactions for categorical and ordinal exposures with three levels. Biometrika 97 , 647–659. (10.1093/biomet/asq030) PubMed DOI PMC
Ives A, Dinnage R, Nell LA, M H, Li D. 2020. Phyr: model based phylogenetic analysis. R package version 1.1.0. See https://github.com/daijiang/phyr/.
Burnham KP, Anderson DR. 2001. Kullback–Leibler information as a basis for strong inference in ecological studies. Wildl. Res. 28 , 111. (10.1071/WR99107) DOI
Quinn GP, Keough MJ. 2002. Experimental design and data analysis for biologists. Cambridge, UK: Cambridge University Press.
Hargitai R, Moskát C, Bán M, Gil D, López‐Rull I, Solymos E. 2010. Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism? J. Avian Biol. 41 , 177–185. (10.1111/j.1600-048X.2009.04818.x) DOI
Spottiswoode CNS, 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
Grim T, Rutila J, Cassey P, Hauber ME. 2009. Experimentally constrained virulence is costly for common cuckoo chicks. Ethology 115 , 14–22. (10.1111/j.1439-0310.2008.01574.x) DOI
Anderson MG, Moskát C, Bán MS, Grim T, Cassey P, Hauber ME, Iwaniuk A. 2009. Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS One 4 , e7725. (10.1371/journal.pone.0007725) PubMed DOI PMC
Lindström J. 1999. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14 , 343–348. (10.1016/s0169-5347(99)01639-0) PubMed DOI
Prinzinger R, Schmidt M, Dietz V. 1995. Embryogeny of oxygen consumption in 13 altricial and precocial birds. Respir. Physiol. 100 , 283–287. (10.1016/0034-5687(94)00139-Q) PubMed DOI
Attard MRG, Portugal SJ. 2024. Global diversity and adaptations of avian eggshell thickness indices. Ibis 166 , 534–550. (10.1111/ibi.13136) DOI
McClelland SC, Cassey P, Maurer G, Hauber ME, Portugal SJ. 2021. How much calcium to shell out? Eggshell calcium carbonate content is greater in birds with thinner shells, larger clutches and longer lifespans. J. R. Soc. Interface 18 , 20210502. (10.1098/rsif.2021.0502) PubMed DOI PMC
Lyon BE, Eadie JM. 1991. Mode of development and interspecific avian brood parasitism. Behav. Ecol. 2 , 309–318. (10.1093/beheco/2.4.309) DOI
Portugal SJ, Maurer G, Thomas GH, Hauber ME, Grim T, Cassey P. 2014. Nesting behaviour influences species-specific gas exchange across avian eggshells. J. Exp. Biol. 217 , 3326–3332. (10.1242/jeb.103291) PubMed DOI PMC
Magrath RD. 1990. Hatching asynchrony in altricial birds. Biol. Rev. 65 , 587–622. (10.1111/j.1469-185X.1990.tb01239.x) DOI
McClelland SC, Lund J, Dixit T, Hamama S, McClean L, Spottiswoode Cet al. . 2024. Data from: Highly-virulent brood-parasitic species show elevated embryonic metabolic rates at specific stages compared to less virulent and non-parasitic species. Figshare. (10.6084/m9.figshare.c.7449538) PubMed DOI