Abstract
In animals, species differ remarkably in parental care strategies. For instance, male-only care is prevalent in teleost fishes, while biparental care predominates in birds and female-only care is widespread in mammals. Understanding the origin and maintenance of diversified parental care systems is a key challenge in evolutionary ecology. It has been suggested that ecological factors and life-history traits play important roles in the evolution of parental care, but the generality of these predictions has not been investigated across a broad range of taxa. Using phylogenetic comparative analyses and detailed parental care data from 1101 avian species that represent 119 families of 26 orders, here we investigate whether parental strategies are associated with ecological variables (i.e., food type, nest structure, and coloniality) and life-history characteristics (i.e., chick development mode and body size). We show that parental care strategies are in relation to coloniality (solitary, semi-colonial, colonial) and chick development mode (altricial vs. precocial). Colonial and altricial species provide more biparental care than solitary and precocial species, respectively. In contrast, food type (plant, invertebrate, vertebrate), nest structure (open vs. closed), and body size do not covary systematically with parental care patterns in birds. Taken together, our results suggest that living in groups and/or having high-demand offspring are strongly associated with biparental care. Towards the end, we discuss future research directions for the study of parental care evolution.
Significance statement
Animal species differ remarkably in the amount of care parents provide to their offspring and in the distribution of care tasks over the parents. In birds, for example, the young of some species are quite independent from the start, while the young of other species are helpless after hatching, requiring a lot of care. Moreover, either the female or the male does most of the caring in some species, while the parental tasks are shared equally in still other species. To understand the diversified parental care patterns, we applied advanced comparative methods to a large data set comprising over 1000 bird species. The analysis reveals that the parents tend to share their care duties equally when they live in groups and/or have offspring that are born helpless, and that parental care patterns are not associated with diet, nest type or body size. Hence, living in groups and having high-demand offspring seem to play important roles in the evolution of parental care.
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Data availability
All data analyzed in this study are included in the supplementary information files.
References
AlRashidi M, Kosztolányi A, Shobrak M, Küpper C, Székely T (2011) Parental cooperation in an extreme hot environment: natural behaviour and experimental evidence. Anim Behav 82:235–243. https://doi.org/10.1016/j.anbehav.2011.04.019
Andersson M (2005) Evolution of classical polyandry: three steps to female emancipation. Ethology 111:1–23. https://doi.org/10.1111/j.1439-0310.2004.01057.x
Ashbrook K, Wanless S, Harris MP, Hamer KC (2008) Hitting the buffers: conspecific aggression undermines benefits of colonial breeding under adverse conditions. Biol Lett 4:630–633. https://doi.org/10.1098/rsbl.2008.0417
Balshine S (2012) Patterns of parental care in vertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, pp 62–80
Barta Z, Székely T, Liker A, Harrison F (2014) Social role specialization promotes cooperation between parents. Am Nat 183:747–761. https://doi.org/10.1086/676014
Barve S, La Sorte FA (2016) Fruiting season length restricts global distribution of female-only parental care in frugivorous passerine birds. PLoS One 11:e0154871. https://doi.org/10.1371/journal.pone.0154871
Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life history, mating system and extinction. Oxford University Press, Oxford
Brown JL, Morales V, Summers K (2010) A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am Nat 175:436–446. https://doi.org/10.1086/650727
Brown CR, Brown MB (2001) Avian coloniality. In: Nolan V and Thompson CF (eds) Current ornithology. Springer, Boston, pp 1–82. https://doi.org/10.1007/978-1-4615-1211-0_1
Bulla M, Prüter H, Vitnerová H, Tijsen W, Sládeček M, Alves JA, Gilg O, Kempenaers B (2017) Flexible parental care: uniparental incubation in biparentally incubating shorebirds. Sci Rep 7:12851. https://doi.org/10.1038/s41598-017-13005-y
Carey C (2002) Incubation in extreme environments. In: Deeming DC (ed) Avian Incubation: Behaviour, Environment, and Evolution. Oxford University Press, Oxford, pp 238–253
Choudhury S (1995) Divorce in birds: a review of the hypotheses. Anim Behav 50:413–429. https://doi.org/10.1006/anbe.1995.0256
Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc Lond B 273:1375–1383. https://doi.org/10.1098/rspb.2005.3458
Cockle KL, Bodrati A (2017) Divergence in nest placement and parental care of Neotropical foliage-gleaners and treehunters (Furnariidae: Philydorini). J Field Ornithol 88:336–348. https://doi.org/10.1111/jofo.12227
Collias N, Collias E (1984) Nest building behavior in birds. Princeton University Press, Princeton
Cooney CR, Sheard C, Clark AD et al (2020) Ecology and allometry predict the evolution of avian developmental durations. Nat Commun 11:2383. https://doi.org/10.1038/s41467-020-16257-x
Coulson JC (2002) Colonial breeding in seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 87–113
Crook JH (1964) The evolution of social organisation and visual communication in the weaver birds (Ploceinae). Behaviour Suppl 10:1–178. https://www.jstor.org/stable/30039146
Danchin E, Wagner RH (1997) The evolution of coloniality: the emergence of new perspectives. Trends Ecol Evol 12:342–347. https://doi.org/10.1016/S0169-5347(97)01124-5
Deeming DC (2011) Importance of nest type on the regulation of humidity in bird nests. Avian Biol Res 4:23–31. https://doi.org/10.3184/175815511X13013963263739
Eberhart-Phillips LJ, Küpper C, Carmona-Isunza MC et al (2018) Demographic causes of adult sex ratio variation and their consequences for parental cooperation. Nat Commun 9:1651. https://doi.org/10.1038/s41467-018-03833-5
Eldegard K, Sonerud GA (2009) Female offspring desertion and male-only care increase with natural and experimental increase in food abundance. Proc R Soc Lond B 276:1713–1721. https://doi.org/10.1098/rspb.2008.1775
Fang YT, Tuanmu MN, Hung CM (2018) Asynchronous evolution of interdependent nest characters across the avian phylogeny. Nat Commun 9:1863. https://doi.org/10.1038/s41467-018-04265-x
Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726. https://doi.org/10.1086/343873
Gilbert JD, Manica A (2010) Parental care trade-offs and life-history relationships in insects. Am Nat 176:212–226. https://doi.org/10.1086/653661
Gochfeld M (1980) Mechanisms and adaptive value of reproductive synchrony in colonial seabirds. In: Burger J, Olla BL, Winn HE (eds) Behavior of marine animals. Springer, Boston, pp 207–270. https://doi.org/10.1007/978-1-4684-2988-67
Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge
Houston AI, Székely T, McNamara JM (2005) Conflict between parents over care. Trends Ecol Evol 20:33–38. https://doi.org/10.1016/j.tree.2004.10.008
Hunt GR, Holzhaider JC, Gray RD (2012) Prolonged parental feeding in tool-using New Caledonian crows. Ethology 118:423–430. https://doi.org/10.1111/j.1439-0310.2012.02027.x
Jeschke JM, Kokko H (2008) Mortality and other determinants of bird divorce rate. Behav Ecol Sociobiol 63:1–9. https://doi.org/10.1007/s00265-008-0646-9
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448. https://doi.org/10.1038/nature11631
Kiester AR, Slatkin M (1974) A strategy of movement and resource utilization. Theor Popul Biol 6:1–20. https://doi.org/10.1016/0040-5809(74)90028-8
Klug H, Bonsall MB (2010) Life history and the evolution of parental care. Evolution 64:823–835. https://doi.org/10.1111/j.1558-5646.2009.00854.x
Klug H, Bonsall MB, Alonzo SH (2013) The origin of parental care in relation to male and female life history. Ecol Evol 3:779–791. https://doi.org/10.1002/ece3.493
Kokko H, Jennions MD (2008) Parental investment, sexual selection and sex ratios. J Evol Biol 21:919–948. https://doi.org/10.1111/j.1420-9101.2008.01540.x
Kölliker M, Brodie ED III, Moore AJ (2005) The coadaptation of parental supply and offspring demand. Am Nat 166:506–516. https://doi.org/10.1086/491687
Kolm N, Goodwin NB, Balshine S, Reynolds JD (2006) Life history evolution in cichlids 1: revisiting the evolution of life histories in relation to parental care. J Evol Biol 19:66–75. https://doi.org/10.1111/j.1420-9101.2005.00984.x
Lack D (1968) Ecological adaptations for breeding in birds. Chapman & Hall, London
Langen TA (2000) Prolonged offspring dependence and cooperative breeding in birds. Behav Ecol 11:367–377. https://doi.org/10.1093/beheco/11.4.367
Lessells CM (2012) Sexual conflict. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, pp 150–170
Liker A, Székely T (2005) Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59:890–897. https://doi.org/10.1111/j.0014-3820.2005.tb01762.x
Liker A, Freckleton RP, Székely T (2013) The evolution of sex roles in birds is related to adult sex ratio. Nat Commun 4:1587. https://doi.org/10.1038/ncomms2600
Liker A, Freckleton RP, Remeš V, Székely T (2015) Sex differences in parental care: gametic investment, sexual selection, and social environment. Evolution 69:2862–2875. https://doi.org/10.1111/evo.12786
Lindenfors P, Revell LJ, Nunn CL (2010) Sexual dimorphism in primate aerobic capacity: a phylogenetic test. J Evol Biol 23:1183–1194. https://doi.org/10.1111/j.1420-9101.2010.01983.x
Lindstedt SL, Calder WA (1976) Body size and longevity in birds. Condor 78:91–94. https://doi.org/10.2307/1366920
Lindstedt SL, Calder WA (1981) Body size, physiological time, and longevity of homeothermic animals. Q Rev Biol 56:1–16. https://doi.org/10.1086/412080
Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc Lond B 267:2287–2293. https://doi.org/10.1098/rspb.2000.1281
Martin TE, Boyce AJ, Fierro-Calderón K, Mitchell AE, Armstad CE, Mouton JC, Bin Soudi EE (2017) Enclosed nests may provide greater thermal than nest predation benefits compared with open nests across latitudes. Funct Ecol 31:1231–1240. https://doi.org/10.1111/1365-2435.12819
McNamara JM, Székely T, Webb JN, Houston AI (2000) A dynamic game-theoretic model of parental care. J Theor Biol 205:605–623. https://doi.org/10.1006/jtbi.2000.2093
Morton ES (1973) On the evolutionary advantages and disadvantages of fruit eating in tropical birds. Am Nat 107:8–22. https://doi.org/10.1086/282813
Nelson B (1980) Seabirds: their biology and ecology. Hamlyn, London
Newton I (1979) Population ecology of raptors. Poyser, Berkhamsted, UK
Olson VA, Liker A, Freckleton RP, Székely T (2008) Parental conflict in birds: comparative analyses of offspring development, ecology and mating opportunities. Proc R Soc Lond B 275:301–307. https://doi.org/10.1098/rspb.2007.1395
Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Isaac NJB (2012) Package ‘caper’, reference manual, http://cran.r-project.org/web/packages/caper/index.html
Owens IP (2002) Male–only care and classical polyandry in birds: phylogeny, ecology and sex differences in remating opportunities. Proc R Soc Lond B 357:283–293. https://doi.org/10.1098/rstb.2001.0929
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. https://doi.org/10.1038/44766
Parker G, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Phil Trans R Soc B 357:295–307. https://doi.org/10.1098/rstb.2001.0950
Perrins CM, Birkhead TR (1983) Avian ecology. Blackie, Glasgow, UK
Pilakouta N, Hanlon EJ, Smiseth PT (2018) Biparental care is more than the sum of its parts: experimental evidence for synergistic effects on offspring fitness. Proc R Soc B 285:20180875. https://doi.org/10.1098/rspb.2018.0875
R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org
Ratz T, Kremi K, Leissle L, Richardson J, Smiseth PT (2021) Access to resources shapes sex differences between caring parents. Front Ecol Evol 9:712425. https://doi.org/10.3389/fevo.2021.712425
Remeš V, Freckleton RP, Tökölyi J, Liker A, Székely T (2015) The evolution of parental cooperation in birds. P Natl Acad Sci USA 112:13603–13608. https://doi.org/10.1073/pnas.1512599112
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Reynolds JD, Székely T (1997) The evolution of parental care in shorebirds: life histories, ecology, and sexual selection. Behav Ecol 8:126–134. https://doi.org/10.1093/beheco/8.2.126
Russell EM, Yom-Tov Y, Geffen E (2004) Extended parental care and delayed dispersal: northern, tropical, and southern passerines compared. Behav Ecol 15:831–838. https://doi.org/10.1093/beheco/arh088
Skutch AF (1949) Do tropical birds rear as many young as they can nourish? Ibis 91:430–455. https://doi.org/10.1111/j.1474-919X.1949.tb02293.x
Slagsvold T, Sonerud GA (2007) Prey size and ingestion rate in raptors: importance for sex roles and reversed sexual size dimorphism. J Avian Biol 38:650–661. https://doi.org/10.1111/j.2007.0908-8857.04022.x
Starck JM, Ricklefs RE (1998) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, Oxford
Stearns SC (1976) Life-history tactics: a review of the ideas. Q Rev Biol 51:3–47. https://doi.org/10.1086/409052
Székely T, Reynolds JD (1995) Evolutionary transitions in parental care in shorebirds. Proc R Soc Lond B 262:57–64. https://doi.org/10.1098/rspb.1995.0176
Temrin H, Tullberg BS (1995) A phylogenetic analysis of the evolution of avian mating systems in relation to altricial and precocial young. Behav Ecol 6:296–307. https://doi.org/10.1093/beheco/6.3.296
Thomas GH, Székely T (2005) Evolutionary pathways in shorebird breeding systems: sexual conflict, parental care, and chick development. Evolution 59:2222–2230. https://doi.org/10.1111/j.0014-3820.2005.tb00930.x
Thomas GH, Freckleton RP, Székely T (2006) Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds. Proc R Soc Lond B 273:1619–1624. https://doi.org/10.1098/rspb.2006.3488
Trumbo ST (2012) Patterns of parental care in invertebrates. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, pp 81–100
Tumulty J, Morales V, Summers K (2014) The biparental care hypothesis for the evolution of monogamy: experimental evidence in an amphibian. Behav Ecol 25:262–270. https://doi.org/10.1093/beheco/art116
Vági B, Végvári Z, Liker A, Freckleton RP, Székely T (2019) Parental care and the evolution of terrestriality in frogs. Proc R Soc B 286:20182737. https://doi.org/10.1098/rspb.2018.2737
van Dijk RE, Brinkhuizen DM, Székely T, Komdeur J (2010) Parental care strategies in Eurasian penduline tit are not related to breeding densities and mating opportunities. Behaviour 147:1551–1565. https://doi.org/10.1163/000579510X505454
van Dijk RE, Székely T, Komdeur J, Pogány Á, Fawcett TW, Weissing FJ (2012) Individual variation and the resolution of conflict over parental care in penduline tits. Proc R Soc Lond B 279:1927–1936. https://doi.org/10.1098/rspb.2011.2297
van Turnhout CA, Foppen RP, Leuven RS, van Strien A, Siepel H (2010) Life-history and ecological correlates of population change in Dutch breeding birds. Biol Conserv 143:173–181. https://doi.org/10.1016/j.biocon.2009.09.023
Varela SAM, Danchin E, Wagner RH (2007) Does predation select for or against avian coloniality? A comparative analysis. J Evol Biol 20:1490–1503. https://doi.org/10.1111/j.1420-9101.2007.01334.x
Vleck CM, Hoyt DF, Vleck D (1979) Metabolism of avian embryos: patterns in altricial and precocial birds. Physiol Zool 52:363–1377. https://doi.org/10.1086/physzool.52.3.30155757
West GB, Brown JH, Enquist BJ (2001) A general model for ontogenetic growth. Nature 413:628–631. https://doi.org/10.1038/35098076
Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690. https://doi.org/10.1086/282461
Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz W (2014) EltonTraits 1.0: Species-level foraging attributes of the world’s birds and mammals: Ecological Archives E095–178. Ecology 95:2027. https://doi.org/10.1890/13-1917.1
Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge, Massachusetts
Wong JWY, Meunier J, Kölliker M (2013) The evolution of parental care in insects: the roles of ecology, life history and the social environment. Ecol Entomol 38:123–137. https://doi.org/10.1111/een.12000
Acknowledgements
We appreciate that Zsolt Végvári helped with statistical analysis. We sincerely thank the Center for Information Technology of the University of Groningen for their support and for providing access to the Peregrine high performance computing cluster. We are very grateful to Dustin Rubenstein and two anonymous reviewers for their constructive comments and suggestions on previous versions of the manuscript.
Funding
This work was supported by the PhD fellowship of the Chinese Scholarship Council (No. 201606380125) to XL. YL was supported by Open Fund of Key Laboratory of Biodiversity Science and Ecological Engineering, Ministry of Education. AL was funded by an NKFIH grant (KH 130430) and by the NKFIH’s TKP2020-IKA-07 project financed under the 2020–4.1.1-TKP2020 Thematic Excellence Programme by the National Research, Development and Innovation Fund of Hungary. JK was funded by Netherlands Organization for Scientific Research; NWO (top grant (854.11.003) and ALW grant (823.01.014)). TS was funded by the Royal Society (Wolfson Merit Award WM170050, APEX APX\R1\191045), the Leverhulme Trust (RF/2/RFG/2005/0279, ID200660763), and by the National Research, Development and Innovation Office of Hungary (ÉLVONAL KKP-126949, K-116310).
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All authors conceived the study. XL and AL collected the data. XL conducted the data analyses with inputs from AL. All authors interpreted the results. XL wrote the manuscript, and others contributed important edits.
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Long, X., Liu, Y., Liker, A. et al. Does ecology and life history predict parental cooperation in birds? A comparative analysis. Behav Ecol Sociobiol 76, 92 (2022). https://doi.org/10.1007/s00265-022-03195-5
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DOI: https://doi.org/10.1007/s00265-022-03195-5