Adaptation and constraint shape the evolution of growth patterns in passerine birds across the globe

. 2020 ; 17 () : 29. [epub] 20200930

Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33005206

BACKGROUND: Growth trajectories should be adapted to selective factors of each species' environment. However, major shaping forces of growth and development are unclear, especially when studying several traits at once. Birds provide an ideal opportunity to analyze growth patterns across species due to there being enough available data. We tested the relative importance of nest predation risk, the number of care-givers, nest height, foraging substrate, clutch size, and latitude on growth patterns of passerine birds (Passeriformes) using phylogenetic comparative methods. Specifically, we studied the evolution of fledging time, average and peak growth rates, and relative development at fledging of body mass and tarsus, wing, and tail length. RESULTS: Using a comprehensive literature search and data quality control, we obtained data on growth in 231 species based on 295 populations. Species with long development in the nest grew slowly and had well-developed traits at fledging. Species breeding under high nest predation risk, building their nests close to the ground, and those living in northern temperate regions fledged early and grew fast, sometimes fledging with less developed body mass and traits critical for locomotion (tarsus, wing, and tail). On the other hand, the number of caring adults, clutch size, and species' foraging substrate had very limited predictive value for growth patterns across passerine species. CONCLUSIONS: Shortening of the nestling period was a primary means of accelerating development (in relation to nest predation, nest height, and latitude), sometimes supplemented by higher peak growth rates of body mass, tarsus, and wing (especially in relation to latitude). Overall growth patterns of passerines were adaptively tuned to nest predation risk and nest height, with northern temperate species having especially short nestling periods and fast growth rates of body mass, tarsus, and wing.

Zobrazit více v PubMed

Gilbert SF, Epel D. Ecological Developmental Biology. Sunderland: Sinauer Associates; 2008.

Wainwright PC, Reilly SM. Ecological morphology: integrative organismal biology. Chicago: University of Chicago Press; 1994.

Pigot AL, Sheard C, Miller ET, Bregman TP, Freeman BG, Roll U, et al. Macroevolutionary convergence connects morphological form to ecological function in birds. Nat Ecol Evol. 2020;4:230–239. doi: 10.1038/s41559-019-1070-4. PubMed DOI

Norberg UM. How a long tail and changes in mass and wing shape affect the cost for flight in animals. Funct Ecol. 1995;9:48–54. doi: 10.2307/2390089. DOI

Zeffer A, Johansson LC, Marmebro Å. Functional correlation between habitat use and leg morphology in birds (Aves) Biol J Linn Soc. 2003;79:461–484. doi: 10.1046/j.1095-8312.2003.00200.x. DOI

Esquerré D, Sherratt E, Keogh JS. Evolution of extreme ontogenetic allometric diversity and heterochrony in pythons, a clade of giant and dwarf snakes. Evolution. 2017;71:2829–2844. doi: 10.1111/evo.13382. PubMed DOI

Van Allen B, Briggs V, McCoy M, Vonesh J. Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs. Oecologia. 2010;164:891–898. doi: 10.1007/s00442-010-1728-8. PubMed DOI

Remeš V, Matysioková B. Survival to independence in relation to pre-fledging development and latitude in songbirds across the globe. J Avian Biol. 2016;47:610–618. doi: 10.1111/jav.00841. DOI

Arendt JD. Adaptive intrinsic growth rates: an integration across taxa. Q Rev Biol. 1997;72:149–177. doi: 10.1086/419764. DOI

Mainwaring MC, Hartley IR. Causes and consequences of differential growth in birds. A Behavioral Perspective. Adv Study Behav. 2012;44:225–277. doi: 10.1016/B978-0-12-394288-3.00006-X. DOI

Cheng Y-R, Martin TE. Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk? Am Nat. 2012;180:285–295. doi: 10.1086/667214. PubMed DOI

O’Connor RJ. The growth and development of birds. Chichester: Wiley; 1984.

Starck JM, Ricklefs RE. Avian growth and development: evolution within the Altricial-Precocial Spectrum. Oxford: Oxford University Press; 1998.

Remeš V, Martin TE. Environmental influences on the evolution of growth and developmental rates in passerines. Evolution. 2002;56:2505–2518. doi: 10.1111/j.0014-3820.2002.tb00175.x. PubMed DOI

Martin TE, Lloyd P, Bosque C, Barton DC, Biancucci AL, Cheng Y, et al. Growth rate variation among passerine species in tropical and temperate sites: an antagonistic interaction between parental fod provisioning and nest predation risk. Evolution. 2011;65:1607–1622. doi: 10.1111/j.1558-5646.2011.01227.x. PubMed DOI

Martin TE. Age-related mortality explains life history strategies of tropical and temperate songbirds. Science. 2015;349:966–970. doi: 10.1126/science.aad1173. PubMed DOI

Roff DA, Remeš V, Martin TE. The evolution of fledging age in songbirds. J Evol Biol. 2005;18:1425–1433. doi: 10.1111/j.1420-9101.2005.00958.x. PubMed DOI

Martin TE. A conceptual framework for clutch-size evolution in songbirds. Am Nat. 2014;183:313–324. doi: 10.1086/674966. PubMed DOI

Jones TM, Benson TJ, Ward MP. Does the size and developmental stage of traits at fledging reflect juvenile flight ability among songbirds? Funct Ecol. 2020;34:799–810. doi: 10.1111/1365-2435.13513. DOI

Harmáčková L, Remeš V. The evolution of clutch size in Australian songbirds in relation to climate, predation, and nestling development. Emu-Austral Ornithol. 2017;117:333–343. doi: 10.1080/01584197.2017.1338112. DOI

Martin TE, Tobalske B, Riordan MM, Case SB, Dial KP. Age and performance at fledging are a cause and consequence of juvenile mortality between life stages. Sci Adv. 2018;4:eaar1988. doi: 10.1126/sciadv.aar1988. PubMed DOI PMC

Ton R, Martin TE. Metabolism correlates with variation in post-natal growth rate among songbirds at three latitudes. Funct Ecol. 2016;30:743–748. doi: 10.1111/1365-2435.12548. DOI

Ricklefs RE. Patterns of growth in birds. Ibis. 1968;110:419–451. doi: 10.1111/j.1474-919X.1968.tb00058.x. DOI

Bortolotti GR. Evolution of growth-rates in eagles: sibling competition vs. energy considerations. Ecology. 1986;67:182–194. doi: 10.2307/1938517. DOI

Harrison F, Barta Z, Cuthill I, Székely T. How is sexual conflict over parental care resolved? A meta-analysis. J Evol Biol. 2009;22:1800–1812. doi: 10.1111/j.1420-9101.2009.01792.x. PubMed DOI

Reyer HU. Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.) Behav Ecol Sociobiol. 1980;6:219–227. doi: 10.1007/BF00569203. DOI

Hatchwell BJ. Investment strategies of breeders in avian cooperative breeding systems. Am Nat. 1999;154:205–219. doi: 10.1086/303227. PubMed DOI

Strickland D, Waite TA. Does initial suppression of allofeeding in small jays help to conceal their nests? Can J Zool. 2001;79:2128–2146. doi: 10.1139/z01-171. DOI

Woxvold IA, Magrath MJL. Helping enhances multiple components of reproductive success in the cooperatively breeding apostlebird. J Anim Ecol. 2005;74:1039–1050. doi: 10.1111/j.1365-2656.2005.01001.x. DOI

Naef-Daenzer B, Grüebler MU. Post-fledging survival of altricial birds: ecological determinants and adaptation. J Field Ornithol. 2016;87:227–250. doi: 10.1111/jofo.12157. DOI

Bize P, Metcalfe NB, Roulin A. Catch-up growth strategies differ between body structures: interactions between age and structure-specific growth in wild nestling Alpine swifts. Funct Ecol. 2006;20:857–864. doi: 10.1111/j.1365-2435.2006.01157.x. DOI

Goodpaster S, Ritchison G. Facultative adjustment of pre-fledging mass recession by nestling chimney swifts Chaetura pelagica. J Avian Biol. 2014;45:247–252. doi: 10.1111/jav.00326. DOI

Callan LM, La Sorte FA, Martin TE, Rohwer VG. Higher Nest predation favors rapid fledging at the cost of plumage quality in nestling birds. Am Nat. 2019;193:717–724. doi: 10.1086/702856. PubMed DOI

Wiersma P, Muñoz-Garcia A, Walker A, Williams JB. Tropical birds have a slow pace of life. Proc Natl Acad Sci U S A. 2007;104:9340–9345. doi: 10.1073/pnas.0702212104. PubMed DOI PMC

Ricklefs RE. Growth rates of birds in the humid New World tropics. Ibis. 1976;118:179–207. doi: 10.1111/j.1474-919X.1976.tb03065.x. DOI

Martin TE, Riordan MM, Repin R, Mouton JC, Blake WM. Apparent annual survival estimates of tropical songbirds better reflect life history variation when based on intensive field methods. Glob Ecol Biogeogr. 2017;26:1386–1397. doi: 10.1111/geb.12661. DOI

Matysioková B, Remeš V. Evolution of parental activity at the nest is shaped by the risk of nest predation and ambient temperature across bird species. Evolution. 2018;72:2214–2224. doi: 10.1111/evo.13580. PubMed DOI

Remeš V. Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater) Evolution. 2006;60:1692–1700. doi: 10.1111/j.0014-3820.2006.tb00513.x. PubMed DOI

Remeš V. Avian growth and development rates and age-specific mortality: the roles of nest predation and adult mortality. J Evol Biol. 2007;20:320–325. doi: 10.1111/j.1420-9101.2006.01191.x. PubMed DOI

Matysioková B, Cockburn A, Remeš V. Male incubation feeding in songbirds responds differently to nest predation risk across hemispheres. Anim Behav. 2011;82:1347–1356. doi: 10.1016/j.anbehav.2011.09.018. DOI

Matysioková B, Remeš V. The importance of having a partner: male help releases females from time limitation during incubation in birds. Front Zool. 2014;11:24. doi: 10.1186/1742-9994-11-24. PubMed DOI PMC

Remeš V, Matysioková B, Cockburn A. Nest predation in New Zealand songbirds: exotic predators, introduced prey and long-term changes in predation risk. Biol Conserv. 2012;148:54–60. doi: 10.1016/j.biocon.2012.01.063. DOI

Remeš V, Matysioková B, Cockburn A. Long-term and large-scale analyses of nest predation patterns in Australian songbirds and a global comparison of nest predation rates. J Avian Biol. 2012;43:435–444. doi: 10.1111/j.1600-048X.2012.05599.x. DOI

Tjørve KMC, Tjørve E. Shapes and functions of bird-growth models: how to characterise chick postnatal growth. Zoology. 2010;113:326–333. doi: 10.1016/j.zool.2010.05.003. PubMed DOI

Tjørve KMC, Tjørve E. Modelling avian growth with the unified-Richards: as exemplified by wader-chick growth. J Avian Biol. 2017;48:770–784. doi: 10.1111/jav.00992. DOI

Vrána J, Remeš V, Matysioková B, Tjørve KMC, Tjørve E. Choosing the right sigmoid growth function using the unified-models approach. Ibis. 2019;161:13–26. doi: 10.1111/ibi.12592. DOI

Tjørve KMC, Tjørve E. A proposed family of unified models for sigmoidal growth. Ecol Model. 2017;359:117–127. doi: 10.1016/j.ecolmodel.2017.05.008. DOI

Austin SH, Robinson TR, Robinson WD, Ricklefs RE. Potential biases in estimating the rate parameter of sigmoid growth functions. Methods Ecol Evol. 2011;2:43–51. doi: 10.1111/j.2041-210X.2010.00055.x. DOI

Paine CET, Marthews TR, Vogt DR, Purves D, Rees M, Hector A, et al. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods Ecol Evol. 2012;3:245–256. doi: 10.1111/j.2041-210X.2011.00155.x. DOI

Pommerening A, Muszta A. Relative plant growth revisited: Towards a mathematical standardisation of separate approaches. Ecol Model. 2016;320:383–392. doi: 10.1016/j.ecolmodel.2015.10.015. DOI

Hirst AG, Forster J. When growth models are not universal: evidence from marine invertebrates. Proc R Soc B Biol Sci. 2013;280:20131546. doi: 10.1098/rspb.2013.1546. PubMed DOI PMC

Turnbull LA, Philipson CD, Purves DW, Atkinson RL, Cunniff J, Goodenough A, et al. Plant growth rates and seed size: a re-evaluation. Ecology. 2012;93:1283–1289. doi: 10.1890/11-0261.1. PubMed DOI

Houghton J, Thompson K, Rees M. Does seed mass drive the differences in relative growth rate between growth forms? Proc R Soc B Biol Sci. 2013;280:20130921. doi: 10.1098/rspb.2013.0921. PubMed DOI PMC

Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AØ. The global diversity of birds in space and time. Nature. 2012;491:444–448. doi: 10.1038/nature11631. PubMed DOI

Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC

Symonds MRE, Blomberg SP. A primer on phylogenetic generalised least squares. In: Garamszegi LZ, editor. Mod phylogenetic comp methods their Appl Evol biol. Berlin: Springer; 2014. pp. 105–130.

Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI

Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Isaac NJB, et al. caper: Comparative analyses of phylogenetics and evolution in R. R package version 1.0.1. 2018.

Mundry R. Statistical issues and assumptions of phylogenetic generalized least squares. In: Garamszegi LZ, editor. Mod phylogenetic comp methods their Appl Evol biol. Berlin: Springer; 2014. pp. 131–156.

Wolak ME, Fairbairn DJ, Paulsen YR. Guidelines for estimating repeatability. Methods Ecol Evol. 2012;3:129–137. doi: 10.1111/j.2041-210X.2011.00125.x. DOI

Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw. 2010;33:1–22. doi: 10.18637/jss.v033.i02. PubMed DOI

Schielzeth H. Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol. 2010;1:103–113. doi: 10.1111/j.2041-210X.2010.00012.x. DOI

Martin TE, Oteyza JC, Mitchell AE, Potticary AL, Lloyd P. Postnatal growth rates covary weakly with embryonic development rates and do not explain adult mortality probability among songbirds on four continents. Am Nat. 2015;185:380–389. doi: 10.1086/679612. PubMed DOI

Sofaer HR, Sillett TS, Yoon J, Power ML, Morrison SA, Ghalambor CK. Offspring growth and mobility in response to variation in parental care: a comparison between populations. J Avian Biol. 2018;49:e01646. doi: 10.1111/jav.01646. DOI

Legge S. Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav. 2000;59:1009–1018. doi: 10.1006/anbe.2000.1382. PubMed DOI

Russell AF, Langmore NE, Cockburn A, Astheimer LB, Kilner RM. Reduced egg Investment can conceal helper effects in cooperatively breeding birds. Science. 2007;317:941–4. PubMed

Tjørve KMC, García-Peña GE, Székely T. Chick growth rates in Charadriiformes: comparative analyses of breeding climate, development mode and parental care. J Avian Biol. 2009;40:553–558. doi: 10.1111/j.1600-048X.2009.04661.x. DOI

Tjørve KMC. Does chick development relate to breeding latitude in waders and gulls? Wader Study Gr Bull. 2007;112:12–23.

Sanz JJ. Does daylength explain the latitudinal variation in clutch size of pied flycatchers Ficedula hypoleuca? Ibis. 1999;141:100–108. doi: 10.1111/j.1474-919X.1999.tb04268.x. DOI

Rose AP, Lyon BE. Day length, reproductive effort, and the avian latitudinal clutch size gradient. Ecology. 2013;94:1327–1337. doi: 10.1890/12-0953.1. PubMed DOI

Sofaer HR, Chapman PL, Sillett TS, Ghalambor CK. Advantages of nonlinear mixed models for fitting avian growth curves. J Avian Biol. 2013;44:469–478.

Sofaer HR, Nagle L, Sillett TS, Yoon J, Ghalambor CK. The importance of nighttime length to latitudinal variation in avian incubation attentiveness. J Avian Biol. 2020;51:e02319. doi: 10.1111/jav.02319. DOI

Mace R. A comparison of great tits’ (Parus major) use of time in different daylengths at three European sites. J Anim Ecol. 1989;58:143–151. doi: 10.2307/4991. DOI

Sanz JJ, Tinbergen JM, Moreno J, Orell M, Verhulst S. Latitudinal variation in parental energy expenditure during brood rearing in the great tit. Oecologia. 2000;122:149–154. doi: 10.1007/PL00008842. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...