The evolution of parental cooperation in birds
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
26483476
PubMed Central
PMC4640770
DOI
10.1073/pnas.1512599112
PII: 1512599112
Knihovny.cz E-resources
- Keywords
- behavior, climate, parental care, sex ratio, sexual selection,
- MeSH
- Biological Evolution * MeSH
- Species Specificity MeSH
- Phylogeny MeSH
- Sex Ratio MeSH
- Birds physiology MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Parental care is one of the most variable social behaviors and it is an excellent model system to understand cooperation between unrelated individuals. Three major hypotheses have been proposed to explain the extent of parental cooperation: sexual selection, social environment, and environmental harshness. Using the most comprehensive dataset on parental care that includes 659 bird species from 113 families covering both uniparental and biparental taxa, we show that the degree of parental cooperation is associated with both sexual selection and social environment. Consistent with recent theoretical models parental cooperation decreases with the intensity of sexual selection and with skewed adult sex ratios. These effects are additive and robust to the influence of life-history variables. However, parental cooperation is unrelated to environmental factors (measured at the scale of whole species ranges) as indicated by a lack of consistent relationship with ambient temperature, rainfall or their fluctuations within and between years. These results highlight the significance of social effects for parental cooperation and suggest that several parental strategies may coexist in a given set of ambient environment.
Department of Animal and Plant Sciences University of Sheffield Sheffield S10 2TN United Kingdom;
Department of Limnology University of Pannonia H 8201 Veszprém Hungary;
Department of Zoology and Laboratory of Ornithology Palacky University 77146 Olomouc Czech Republic;
See more in PubMed
Clutton-Brock TH. The Evolution of Parental Care. Princeton University Press; Princeton: 1991.
Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012.
McGraw L, Székely T, Young LJ. In: Pair bonds and parental behaviour. Social Behaviour: Genes, Ecology and Evolution. Székely T, Moore AJ, Komdeur J, editors. Cambridge University Press; Cambridge: 2010. pp. 271–301.
Balshine S. Patterns of parental care in vertebrates. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 62–80.
Trumbo ST. Patterns of parental care in invertebrates. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 81–100.
Lessells CM. Sexual conflict. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 150–170.
Klug H, Alonzo SH, Bonsall MB. Theoretical foundations of parental care. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 21–39.
Mcnamara JM, Székely T, Webb JN, Houston AI. A dynamic game-theoretic model of parental care. J Theor Biol. 2000;205(4):605–623. PubMed
Harrison F, Barta Z, Cuthill I, Székely T. How is sexual conflict over parental care resolved? A meta-analysis. J Evol Biol. 2009;22(9):1800–1812. PubMed
Barta Z, Székely T, Liker A, Harrison F. Social role specialization promotes cooperation between parents. Am Nat. 2014;183(6):747–761. PubMed
McNamara JM, Wolf M. Sexual conflict over parental care promotes the evolution of sex differences in care and the ability to care. Proc R Soc London B. 2015;282(1803):20142752. PubMed PMC
Wilson EO. Sociobiology: The New Synthesis. Harvard University Press; Cambridge: 1975.
Olson VA, Liker A, Freckleton RP, Székely T. Parental conflict in birds: Comparative analyses of offspring development, ecology and mating opportunities. Proc Biol Sci. 2008;275(1632):301–307. PubMed PMC
Webb TJ, Olson VA, Székely T, Freckleton RP. Who cares? Quantifying the evolution of division of parental effort. Methods Ecol Evol. 2010;1(3):221–230.
Andersson M. Sexual Selection. Princeton University Press; Princeton: 1994.
Adrian O, Brockmann I, Hohoff C, Sachser N. Paternal behaviour in wild guinea pigs: A comparative study in three closely related species with different social and mating systems. J Zool (Lond) 2005;265(1):97–105.
Queller DC. Why do females care more than males? Proc Biol Sci. 1997;264(1388):1555–1557.
Gonzalez-Voyer A, Fitzpatrick JL, Kolm N. Sexual selection determines parental care patterns in cichlid fishes. Evolution. 2008;62(8):2015–2026. PubMed
Jennions MD, Kokko H. Sexual selection. In: Westneat DF, Fox CW, editors. Evolutionary Behavioral Ecology. Oxford University Press; Oxford: 2010. pp. 343–364.
Magrath MJL, Komdeur J. Is male care compromised by additional mating opportunity? Trends Ecol Evol. 2003;18(8):424–430.
Kokko H. Cuckoldry and the stability of biparental care. Ecol Lett. 1999;2(4):247–255.
Sheldon BC. Relating paternity to paternal care. Philos Trans R Soc Lond B Biol Sci. 2002;357(1419):341–350. PubMed PMC
Kokko H, Jennions MD. Parental investment, sexual selection and sex ratios. J Evol Biol. 2008;21(4):919–948. PubMed
Alonzo SH, Klug H. Paternity, maternity, and parental care. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 189–205.
Griffin AS, Alonzo SH, Cornwallis CK. Why do cuckolded males provide paternal care? PLoS Biol. 2013;11(3):e1001520. PubMed PMC
Forsgren E, Amundsen T, Borg AA, Bjelvenmark J. Unusually dynamic sex roles in a fish. Nature. 2004;429(6991):551–554. PubMed
Liker A, Freckleton RP, Székely T. The evolution of sex roles in birds is related to adult sex ratio. Nat Commun. 2013;4:1587. PubMed
Parra JE, Beltrán M, Zefania S, Dos Remedios N, Székely T. Experimental assessment of mating opportunities in three shorebird species. Anim Behav. 2014;90(4):83–90.
Székely T, Webb JN, Cuthill IC. Mating patterns, sexual selection, and parental care: An integrative approach. In: Apollonio M, Festa-Bianchet M, Mainardi M, editors. Vertebrate Mating Systems. World Scientific Publishing; Singapore: 2000. pp. 159–185.
Kokko H, Jennions MD. Sex differences in parental care. In: Royle NJ, Smiseth PT, Kölliker M, editors. The Evolution of Parental Care. Oxford University Press; Oxford: 2012. pp. 101–118.
Alexander RD. The evolution of social behavior. Annu Rev Ecol Syst. 1974;5:325–383.
Jarman PJ. Social organization of antelope in relation to their ecology. Behaviour. 1974;48(1):215–267.
Rubenstein DR. Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc Natl Acad Sci USA. 2011;108(Suppl 2):10816–10822. PubMed PMC
Jetz W, Rubenstein DR. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr Biol. 2011;21(1):72–78. PubMed
Crook JH. The evolution of social organisation and visual communication in the weaver birds (Ploceinae) Behav. 1964;10(Suppl):1–178.
Leisler B, Winkler H, Wink M. Evolution of breeding systems in acrocephaline warblers. Auk. 2002;119(2):379–390.
Shen S-F, et al. Unfavourable environment limits social conflict in Yuhina brunneiceps. Nat Commun. 2012;3:885. PubMed
Smaldino PE, Schank JC, McElreath R. Increased costs of cooperation help cooperators in the long run. Am Nat. 2013;181(4):451–463. PubMed
Smaldino PE, Newson L, Schank JC, Richerson PJ. Simulating the evolution of the human family: Cooperative breeding increases in harsh environments. PLoS One. 2013;8(11):e80753. PubMed PMC
Székely T, Remeš V, Freckleton RP, Liker A. Why care? Inferring the evolution of complex social behaviour. J Evol Biol. 2013;26(7):1381–1391. PubMed
Freckleton RP, Harvey PH, Pagel M. Phylogenetic analysis and comparative data: A test and review of evidence. Am Nat. 2002;160(6):712–726. PubMed
Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AØ. The global diversity of birds in space and time. Nature. 2012;491(7424):444–448. PubMed
Fairbairn D, Blanckenhorn W, Székely T. Sex, Size and Gender Roles. Oxford University Press; Oxford: 2007.
Lukas D, Clutton-Brock TH. The evolution of social monogamy in mammals. Science. 2013;341(6145):526–530. PubMed
Houston AI, McNamara JM. A self-consistent approach to paternity and parental effort. Philos Trans R Soc Lond B Biol Sci. 2002;357(1419):351–362. PubMed PMC
Matysioková B, Remeš V. Faithful females receive more help: The extent of male parental care during incubation in relation to extra-pair paternity in songbirds. J Evol Biol. 2013;26(1):155–162. PubMed
Møller AP, Birkhead TR. Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol. 1993;33(4):261–268.
Schwagmeyer PL, et al. Species differences in male parental care in birds: A reexamination of correlates with paternity. Auk. 1999;116(2):487–503.
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(1):24. PubMed PMC
Liker A, Székely T. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution. 2005;59(4):890–897. PubMed
Arendt JD, Reznick DN, López-Sepulcre A. Replicated origin of female-biased adult sex ratio in introduced populations of the trinidadian guppy (Poecilia reticulata) Evolution. 2014;68(8):2343–2356. PubMed
Székely T, Liker A, Freckleton RP, Fichtel C, Kapperel PM. Sex-biased survival predicts adult sex ratio variation in wild birds. Proc R Soc London B. 2014;281(1788):20140342. PubMed PMC
Székely T, Weissing FJ, Komdeur J. Adult sex ratio variation: Implications for breeding system evolution. J Evol Biol. 2014;27(8):1500–1512. PubMed
Lehtonen J, Kokko H. Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes. Philos Trans R Soc Lond B Biol Sci. 2012;367(1586):211–221. PubMed PMC
Jeschke JM, Kokko H. Mortality and other determinants of bird divorce rate. Behav Ecol Sociobiol. 2008;63(1):1–9.
Botero CA, Rubenstein DR. Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS One. 2012;7(2):e32311. PubMed PMC
Liker A, Freckleton RP, Székely T. Divorce and infidelity are associated with skewed adult sex ratios in birds. Curr Biol. 2014;24(8):880–884. PubMed
Rubenstein DR, Lovette IJ. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr Biol. 2007;17(16):1414–1419. PubMed
Gonzalez J-CT, Sheldon BC, Tobias JA. Environmental stability and the evolution of cooperative breeding in hornbills. Proc R Soc London B. 2013;280(1768):20131297. PubMed PMC
Friedman NR, Remeš V. 2015. Global geographic patterns of sexual size dimorphism in birds: Support for a latitudinal trend? Ecography, 10.1111/ecog.01531.
Alonzo SH. Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol Evol. 2010;25(2):99–108. PubMed
Head ML, Hinde CA, Moore AJ, Royle NJ. Correlated evolution in parental care in females but not males in response to selection on paternity assurance behaviour. Ecol Lett. 2014;17(7):803–810. PubMed PMC
Dunn PO, Whittingham LA, Pitcher TE. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution. 2001;55(1):161–175. PubMed
Cornwallis CK, West SA, Davis KE, Griffin AS. Promiscuity and the evolutionary transition to complex societies. Nature. 2010;466(7309):969–972. PubMed
Donald PF. Adult sex ratios in wild bird populations. Ibis. 2007;149(4):671–692.
BirdLife International and NatureServe . Bird Species Distribution Maps of the World. BirdLife International, Cambridge, UK and NatureServe; Arlington, VA: 2011.
Freckleton RP. Fast likelihood calculations for comparative analyses. Methods Ecol Evol. 2012;3(5):940–947.
R-Core-Team 2013. R: A language and environment for statistical computing. Available at: www.r-project.org/
Evolution of female promiscuity in Passerides songbirds
Flexible parental care: Uniparental incubation in biparentally incubating shorebirds
Dryad
10.5061/dryad.02JK0