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

. 2024 Sep ; 20 (9) : 20240411. [epub] 20240925

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39317329

Grantová podpora
U54 MD017979 NIMHD NIH HHS - United States
Leverhulme Trust
Natural Environment Research Council

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.

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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

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