Self-recognition, color signals, and cycles of greenbeard mutualism and altruism.

Altruism presents a challenge to evolutionary theory because selection should favor selfish over caring strategies. Greenbeard altruism resolves this paradox by allowing cooperators to identify individuals carrying similar alleles producing a form of genic selection. In side-blotched lizards, genetically similar but unrelated blue male morphs settle on adjacent territories and cooperate. Here we show that payoffs of cooperation depend on asymmetric costs of orange neighbors. One blue male experiences low fitness and buffers his unrelated partner from aggressive orange males despite the potential benefits of defection. We show that recognition behavior is highly heritable in nature, and we map genetic factors underlying color and self-recognition behavior of genetic similarity in both sexes. Recognition and cooperation arise from genome-wide factors based on our mapping study of the location of genes responsible for self-recognition behavior, recognition of blue color, and the color locus. Our results provide an example of greenbeard interactions in a vertebrate that are typified by cycles of greenbeard mutualism interspersed with phases of transient true altruism. Such cycles provide a mechanism encouraging the origin and stability of true altruism.

[1]  J. Dickinson,et al.  Desperately Seeking Similarity , 2003, Science.

[2]  J. Martin Marcos,et al.  Kin Selection in Cooperative Alliances of Carrion Crows , 2003, Science.

[3]  R. Grosberg,et al.  Mate selection and the evolution of highly polymorphic self/nonself recognition genes. , 2000, Science.

[4]  B. Sinervo,et al.  The rock–paper–scissors game and the evolution of alternative male strategies , 1996, Nature.

[5]  E. Lander,et al.  Construction of multilocus genetic linkage maps in humans. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Höglund,et al.  Fine-scale genetic structuring on Manacus manacus leks , 2000, Nature.

[7]  R. Lewontin.  ‘The Selfish Gene’ , 1977, Nature.

[8]  Y. Brandt,et al.  Persistence of individually distinctive display patterns in fatigued side-blotched lizards (Uta stansburiana) , 2003, Behavioral Ecology and Sociobiology.

[9]  H. Moore,et al.  Exceptional sperm cooperation in the wood mouse , 2002, Nature.

[10]  B. Sinervo,et al.  Morphs, Dispersal Behavior, Genetic Similarity, and the Evolution of Cooperation , 2003, Science.

[11]  J. Clobert,et al.  Affinity towards maternal odour and offspring dispersal in the common lizard , 2000 .

[12]  J. Strassmann,et al.  Single-Gene Greenbeard Effects in the Social Amoeba Dictyostelium discoideum , 2003, Science.

[13]  M. Spence,et al.  Analysis of human genetic linkage , 1986 .

[14]  SOCIALLY MEDIATED SPECIATION , 2003 .

[15]  M. Feldman,et al.  Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors , 2002, Nature.

[16]  Barry Sinervo,et al.  Testosterone, Endurance, and Darwinian Fitness: Natural and Sexual Selection on the Physiological Bases of Alternative Male Behaviors in Side-Blotched Lizards , 2000, Hormones and Behavior.

[17]  K. Foster,et al.  Pleiotropy as a mechanism to stabilize cooperation , 2004, Nature.

[18]  P. Sherman,et al.  Self-referent phenotype matching: theoretical considerations and empirical evidence , 2001, Trends in Neurosciences.

[19]  B. Hatchwell,et al.  Kin recognition: function and mechanism in avian societies. , 1999, Trends in ecology & evolution.

[20]  B. Sinervo,et al.  Correlational selection and the evolution of genomic architecture , 2002, Heredity.

[21]  D. Queller,et al.  Computer software for performing likelihood tests of pedigree relationship using genetic markers , 1999, Molecular ecology.

[22]  B. Sinervo,et al.  An experimental test of the ideal despotic distribution , 2002 .

[23]  SOCIAL CAUSES OF CORRELATIONAL SELECTION AND THE RESOLUTION OF A HERITABLE THROAT COLOR POLYMORPHISM IN A LIZARD , 2001, Evolution; international journal of organic evolution.

[24]  Alan H. Krakauer,et al.  Kin selection and cooperative courtship in wild turkeys , 2005, Nature.

[25]  D. Haig,et al.  Gestational drive and the green-bearded placenta. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Ross A Hammond,et al.  ALTRUISM VIA KIN‐SELECTION STRATEGIES THAT RELY ON ARBITRARY TAGS WITH WHICH THEY COEVOLVE , 2004, Evolution; international journal of organic evolution.

[27]  B. Sinervo,et al.  Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  W. Hamilton.  The genetical evolution of social behaviour. I. , 1964, Journal of theoretical biology.

[29]  B. Sinervo,et al.  Uncoupling direct and indirect components of female choice in the wild , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  L. Keller,et al.  Selfish genes: a green beard in the red fire ant , 1998, Nature.