Friday, May 9, 2025
No menu items!
HomeNatureA cryptic role for reciprocal helping in a cooperatively breeding bird

A cryptic role for reciprocal helping in a cooperatively breeding bird

  • Ågren, J. A., Davies, N. G. & Foster, K. R. Enforcement is central to the evolution of cooperation. Nat. Ecol. Evol. 3, 1018–1029 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Brown, J. L. Avian communal breeding systems. Annu. Rev. Ecol. Syst. 9, 123–155 (1978).

    Article 

    Google Scholar
     

  • Riehl, C. Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. B 280, 20132245 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pereira, A. S., De Moor, D., Casanova, C. & Brent, L. J. N. Kinship composition in mammals. R. Soc. Open Sci. 10, 230486 (2023).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kramer, K. L. Cooperative breeding and its significance to the demographic success of humans. Annu. Rev. Anthropol. 39, 417–436 (2010).

    Article 

    Google Scholar
     

  • Cornwallis, C. K., West, S. A. & Griffin, A. S. Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J. Evol. Biol. 22, 2445–2457 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kingma, S. A. Direct benefits explain interspecific variation in helping behaviour among cooperatively breeding birds. Nat. Commun. 8, 1094 (2017).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • García-Ruiz, I., Quiñones, A. & Taborsky, M. The evolution of cooperative breeding by direct and indirect fitness effects. Sci. Adv. 8, eabl7853 (2022).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).

    Article 
    ADS 
    MathSciNet 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Clutton-Brock, T. Cooperation between non-kin in animal societies. Nature 462, 51–57 (2009).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Connor, R. C. Pseudo-reciprocity: investing in mutualism. Anim. Behav. 34, 1562–1566 (1986).

    Article 

    Google Scholar
     

  • Trivers, R. L. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971).

    Article 

    Google Scholar
     

  • Van Cleve, J. & Akçay, E. Pathways to social evolution: reciprocity, relatedness, and synergy. Evolution 68, 2245–2258 (2014).

    PubMed 

    Google Scholar
     

  • Bshary, R., Zuberbühler, K. & Van Schaik, C. P. Why mutual helping in most natural systems is neither conflict-free nor based on maximal conflict. Philos. Trans. R. Soc. B 371, 20150091 (2016).

    Article 

    Google Scholar
     

  • Carter, G. G. Reciprocity versus pseudo‐reciprocity: A false dichotomy. Ethology 130, e13431 (2023).

  • Leimar, O. & Bshary, R. Social bond dynamics and the evolution of helping. Proc. Natl Acad. Sci. USA 121, e2317736121 (2024).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wilkinson, G. S. Reciprocal food sharing in the vampire bat. Nature 308, 181–184 (1984).

    Article 
    ADS 

    Google Scholar
     

  • Wilkinson, G. S. Reciprocal altruism in bats and other mammals. Ethol. Sociobiol. 9, 85–100 (1988).

    Article 

    Google Scholar
     

  • Wiley, R. H. & Rabenold, K. N. The evolution of cooperative breeding by delayed reciprocity and queuing for favorable social positions. Evolution 38, 609–621 (1984).

    Article 
    PubMed 

    Google Scholar
     

  • Ligon, J. D. & Ligon, S. H. Communal breeding in green woodhoopoes as a case for reciprocity. Nature 276, 496–498 (1978).

    Article 
    ADS 

    Google Scholar
     

  • Kern, J. M. & Radford, A. N. Experimental evidence for delayed contingent cooperation among wild dwarf mongooses. Proc. Natl Acad. Sci. USA 115, 6255–6260 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carter, G. G. Co-option and the evolution of food sharing in vampire bats. Ethology 127, 837–849 (2021).

    Article 

    Google Scholar
     

  • Kokko, H., Johnstone, R. A. & Clutton-Brock, T. H. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. B 268, 187–196 (2001).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carter, G. G., Schino, G. & Farine, D. Challenges in assessing the roles of nepotism and reciprocity in cooperation networks. Anim. Behav. 150, 255–271 (2019).

    Article 

    Google Scholar
     

  • West, S. A., Cooper, G. A., Ghoul, M. B. & Griffin, A. S. Ten recent insights for our understanding of cooperation. Nat. Ecol. Evol. 5, 419–430 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shah, S. S. & Rubenstein, D. R. Group augmentation underlies the evolution of complex sociality in the face of environmental instability. Proc. Natl Acad. Sci. USA 120, e2212211120 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guindre-Parker, S. & Rubenstein, D. R. No short-term physiological costs of offspring care in a cooperatively breeding bird. J. Exp. Biol. 221, jeb186569 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Little, J., Rubenstein, D. R. & Guindre-Parker, S. Plasticity in social behaviour varies with reproductive status in an avian cooperative breeder. Proc. R. Soc. B 289, 20220355 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guindre-Parker, S. & Rubenstein, D. R. Multiple benefits of alloparental care in a fluctuating environment. R. Soc. Open Sci. 5, 172406 (2018).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guindre-Parker, S. & Rubenstein, D. R. Survival benefits of group living in a fluctuating environment. Am. Nat. 195, 1027–1036 (2020).

    Article 
    PubMed 

    Google Scholar
     

  • Rubenstein, D. R. Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc. Natl Acad. Sci. USA 108, 10816–10822 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rubenstein, D. R. in Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior (eds Koenig, W. & Dickinson, J.) 181–196 (Cambridge Univ. Press, 2016).

  • Rubenstein, D. R. Territory quality drives intraspecific patterns of extrapair paternity. Behav. Ecol. 18, 1058–1064 (2007).

    Article 

    Google Scholar
     

  • Rubenstein, D. R. Temporal but not spatial environmental variation drives adaptive offspring sex allocation in a plural cooperative breeder. Am. Nat. 170, 155–165 (2007).

    Article 
    PubMed 

    Google Scholar
     

  • Kingma, S. A., Santema, P., Taborsky, M. & Komdeur, J. Group augmentation and the evolution of cooperation. Trends Ecol. Evol. 29, 476–484 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Keen, S. C., Meliza, C. D. & Rubenstein, D. R. Flight calls signal group and individual identity but not kinship in a cooperatively breeding bird. Behav. Ecol. 24, 1279–1285 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ligon, J. D. Cooperation and reciprocity in avian social systems. Am. Nat. 121, 366–384 (1983).

    Article 

    Google Scholar
     

  • Valencia, J., De La Cruz, C. & González, B. Flexible helping behaviour in the azure‐winged magpie. Ethology 109, 545–558 (2003).

    Article 

    Google Scholar
     

  • Dickinson, J. L., Koenig, W. D. & Pitelka, F. A. Fitness consequences of helping behavior in the western bluebird. Behav. Ecol. 7, 168–177 (1996).

    Article 

    Google Scholar
     

  • Lessells, C. M. in Population Biology of Passerine Birds: an Integrated Approach (eds Blondel, J. et al.) 357–368 (Springer, 1990).

  • Emlen, S. T. & Wrege, P. H. A test of alternate hypotheses for helping behavior in white-fronted bee-eaters of Kenya. Behav. Ecol. Sociobiol. 25, 303–319 (1989).

    Article 

    Google Scholar
     

  • Hatchwell, B. J. in Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior (eds Koenig, W. D. & Dickinson, J. L.) 39–57 (Cambridge Univ. Press, 2016).

  • Guindre-Parker, S. & Rubenstein, D. R. The oxidative costs of parental care in cooperative and pair-breeding African starlings. Oecologia 188, 53–63 (2018).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Pfeiffer, T., Rutte, C., Killingback, T., Taborsky, M. & Bonhoeffer, S. Evolution of cooperation by generalized reciprocity. Proc. R. Soc. B 272, 1115–1120 (2005).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gardner, A. & West, S. A. Demography, altruism, and the benefits of budding. J. Evol. Biol. 19, 1707–1716 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bygott, J. D., Bertram, B. C. R. & Hanby, J. P. Male lions in large coalitions gain reproductive advantages. Nature 282, 839–841 (1979).

    Article 
    ADS 

    Google Scholar
     

  • Pollack, L. & Rubenstein, D. R. The fitness consequences of kin-biased dispersal in a cooperatively breeding bird. Biol. Lett. 11, 20150336 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rubenstein, D. R. Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proc. R. Soc. B 274, 1895–1903 (2007).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reyer, H.-U. Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.). Behav. Ecol. Sociobiol. 6, 219–227 (1980).

    Article 

    Google Scholar
     

  • Clarke, M. F. Co-operative breeding by the Australian bell miner Manorina melanophrys Latham: a test of kin selection theory. Behav. Ecol. Sociobiol. 14, 137–146 (1984).

    Article 

    Google Scholar
     

  • Ligon, J. D. & Ligon, S. H. Reciprocity in the green woodhoopoe (Phoeniculus purpureus). Anim. Behav. 31, 480–489 (1983).

    Article 

    Google Scholar
     

  • Pew, J., Muir, P. H., Wang, J. & Frasier, T. R. related: an R package for analysing pairwise relatedness from codominant molecular markers. Mol. Ecol. Resour. 15, 557–561 (2015).

    Article 
    PubMed 

    Google Scholar
     

  • Roberts, G. Cooperation through interdependence. Anim. Behav. 70, 901–908 (2005).

    Article 

    Google Scholar
     

  • Fruteau, C., Voelkl, B., Van Damme, E. & Noë, R. Supply and demand determine the market value of food providers in wild vervet monkeys. Proc. Natl Acad. Sci. USA 106, 12007–12012 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Carter, G. The reciprocity controversy. Anim. Behav. Cogn. 1, 368–386 (2014).

    Article 

    Google Scholar
     

  • Koenig, W. D. Reciprocal altruism in birds: a critical review. Ethol. Sociobiol. 9, 73–84 (1988).

    Article 

    Google Scholar
     

  • Connor, R. C. & Curry, R. L. Helping non-relatives: a role for deceit? Anim. Behav. 49, 389–393 (1995).

    Article 

    Google Scholar
     

  • Heinsohn, R. G. Kidnapping and reciprocity in cooperatively breeding white-winged choughs. Anim. Behav. 41, 1097–1100 (1991).

    Article 

    Google Scholar
     

  • Pardo, M. A., Hayes, C. E., Walters, E. L. & Koenig, W. D. Acorn woodpeckers vocally discriminate current and former group members from nongroup members. Behav. Ecol. 31, 1120–1128 (2020).

    Article 

    Google Scholar
     

  • Humphries, D. J., Nelson-Flower, M. J., Bell, M. B. V., Finch, F. M. & Ridley, A. R. Vocal recognition of former group members, but not unknown kin, in the cooperatively breeding southern pied babbler. Anim. Behav. 201, 109–116 (2023).

    Article 

    Google Scholar
     

  • Riehl, C. Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird. Proc. R. Soc. B 278, 1728–1735 (2011).

    Article 
    PubMed 

    Google Scholar
     

  • Rubenstein, D. R. Stress hormones and sociality: integrating social and environmental stressors. Proc. R. Soc. B 274, 967–975 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shah, S. S. & Rubenstein, D. R. Prenatal environmental conditions underlie alternative reproductive tactics that drive the formation of a mixed-kin cooperative society. Sci. Adv. 8, eabk2220 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Griffiths, R., Double, M. C., Orr, K. & Dawson, R. J. G. A DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ripperger, S. P., Stockmaier, S. & Carter, G. G. Tracking sickness effects on social encounters via continuous proximity sensing in wild vampire bats. Behav. Ecol. 31, 1296–1302 (2020).

    Article 

    Google Scholar
     

  • Farine, D. R. Proximity as a proxy for interactions: issues of scale in social network analysis. Anim. Behav. 104, e1–e5 (2015).

    Article 

    Google Scholar
     

  • Davis, G. H., Crofoot, M. C. & Farine, D. R. Estimating the robustness and uncertainty of animal social networks using different observational methods. Anim. Behav. 141, 29–44 (2018).

    Article 

    Google Scholar
     

  • Bürkner, P.-C. brms: An R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).

  • Lüdecke, D., Ben-Shachar, M., Patil, I., Waggoner, P. & Makowski, D. performance: An R package for assessment, comparison and testing of statistical models. J. Open Source Softw. 6, 3139 (2021).

    Article 
    ADS 

    Google Scholar
     

  • Rubenstein, D. R. Isolation and characterization of polymorphic microsatellite loci in the plural cooperatively breeding superb starling, Lamprotornis superbus. Mol. Ecol. Notes 5, 739–744 (2005).

    Article 
    CAS 

    Google Scholar
     

  • Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).

    Article 
    PubMed 

    Google Scholar
     

  • Weinman, L. R., Solomon, J. W. & Rubenstein, D. R. A comparison of single nucleotide polymorphism and microsatellite markers for analysis of parentage and kinship in a cooperatively breeding bird. Mol. Ecol. Resour. 15, 502–511 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Sinnwell, J. P., Therneau, T. M. & Schaid, D. J. The kinship2 R package for pedigree data. Hum. Hered. 78, 91–93 (2014).

    Article 
    PubMed 

    Google Scholar
     

  • Farine, D. R. & Carter, G. G. Permutation tests for hypothesis testing with animal social network data: problems and potential solutions. Methods Ecol. Evol. 13, 144–156 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.6-4 https://cran.r-project.org/web/packages/vegan/index.html (2022).

  • Farine, D. R. Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol. Evol. 4, 1187–1194 (2013).

    Article 

    Google Scholar
     

  • RELATED ARTICLES

    Most Popular

    Recent Comments