Learned Social Preference in Zebrafish

How social aggregations arise and persist is central to our understanding of evolution, behavior, and psychology. When social groups arise within a species, evolutionary divergence and speciation can result. To understand this diversifying role of social behavior, we must examine the internal and external influences that lead to nonrandom assortment of phenotypes. Many fishes form aggregations called shoals that reduce predation risk while enhancing foraging and reproductive success. Thus, shoaling is adaptive, and signals that maintain shoals are likely to evolve under selection. Given the diversity of pigment patterns among Danio fishes, visual signals might be especially important in mediating social behaviors in this group. Our understanding of pigment pattern development in the zebrafish D. rerio allows integrative analyses of how molecular variation leads to morphological variation among individuals and how morphological variation influences social interactions. Here, we use the zebrafish pigment mutant nacre/mitfa to test roles for genetic and environmental determinants in the development of shoaling preference. We demonstrate that individuals discriminate between shoals having different pigment pattern phenotypes and that early experience determines shoaling preference. These results suggest a role for social learning in pigment pattern diversification in danios.

[1]  G. Turner,et al.  Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[2]  A. Jhingran,et al.  Inland Fishes of India and Adjacent Countries , 1991 .

[3]  A. Amsterdam,et al.  Proviral insertions in the zebrafish hagoromo gene, encoding an F-box/WD40-repeat protein, cause stripe pattern anomalies , 2000, Current Biology.

[4]  SOCIALLY MEDIATED SPECIATION , 2003 .

[5]  R. R. Krausz Living in Groups , 2013 .

[6]  E. Wilson The Insect Societies , 1974 .

[7]  A. Magurran,et al.  The adaptive significance of schooling as an anti-predator defense in fish , 1990 .

[8]  Stephen L. Johnson,et al.  How the zebrafish gets its stripes. , 2001, Developmental biology.

[9]  Stephen L. Johnson,et al.  Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio , 2001, Development Genes and Evolution.

[10]  D. Cannatella,et al.  Multiple, recurring origins of aposematism and diet specialization in poison frogs , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Dowling,et al.  Zebrafish ultraviolet visual pigment: absorption spectrum, sequence, and localization. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Foraging group structure among individuals differing in competitive ability , 1993 .

[13]  C. Goding,et al.  Mitf from neural crest to melanoma: signal transduction and transcription in the melanocyte lineage. , 2000, Genes & development.

[14]  Stephen L. Johnson,et al.  Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. , 1999, Development.

[15]  Louie H. Yang,et al.  The Ecology of Individuals: Incidence and Implications of Individual Specialization , 2002, The American Naturalist.

[16]  Barry Sinervo,et al.  SOCIALLY MEDIATED SPECIATION , 2003, Evolution; international journal of organic evolution.

[17]  T. C. Schneirla Aspects of Stimulation and Organization in Approach/Withdrawal Processes Underlying Vertebrate Behavioral Development , 1965 .

[18]  W. Rainboth Inland fishes of India and adjacent countries , 1994, Reviews in Fish Biology and Fisheries.

[19]  C. Carlson,et al.  Effect of cross-rearing on species identification in zebra fish and pearl danios. , 1982, Developmental psychobiology.

[20]  J. Endler Natural and sexual selection on color patterns in poeciliid fishes , 1983, Environmental Biology of Fishes.

[21]  F. Kullander Phylogeny and species diversity of the South and Southeast Asian cyprinid genus Danio Hamilton (Teleostei, Cyprinidae) , 2001 .

[22]  Stephen L. Johnson,et al.  nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. , 1999, Development.

[23]  C. Darwin The Descent of Man and Selection in Relation to Sex: INDEX , 1871 .

[24]  J. Krause,et al.  The social organization of fish shoals: a test of the predictive power of laboratory experiments for the field , 2000, Biological reviews of the Cambridge Philosophical Society.

[25]  Stephen L. Johnson,et al.  An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. , 2000, Development.

[26]  K. Laland,et al.  Who follows whom? Shoaling preferences and social learning of foraging information in guppies , 1998, Animal Behaviour.

[27]  R. Brooks Sex, Color, and Mate Choice in Guppies , 1998 .

[28]  D. Wake,et al.  The Quarterly Review of Biology INTEGRATING HISTORICAL AND MECHANISTIC BIOLOGY ENHANCES THE STUDY OF ADAPTATION , 2002 .

[29]  Supap Mongkolprasit Checklist of fishes in Thailand , 1997 .

[30]  M. Ryan,et al.  SEXUAL SELECTION IN FEMALE PERCEPTUAL SPACE: HOW FEMALE TUNGARA FROGS PERCEIVE AND RESPOND TO COMPLEX POPULATION VARIATION IN ACOUSTIC MATING SIGNALS , 2003, Evolution; international journal of organic evolution.

[31]  G. Alexander,et al.  Color patterns and species recognition in four closely related species of Lake Malawi cichlid , 2002 .

[32]  Stephen L. Johnson,et al.  Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. , 2000, Developmental biology.

[33]  M. McClure Development and evolution of melanophore patterns in fishes of the genus Danio (Teleostei: Cyprinidae) , 1999, Journal of morphology.

[34]  D. Parichy,et al.  Pigment patterns: fish in stripes and spots , 2003, Current Biology.

[35]  Ian K Quigley,et al.  Pigment pattern formation in zebrafish: A model for developmental genetics and the evolution of form , 2002, Microscopy research and technique.

[36]  A. Kondrashov,et al.  A Low Genomic Number of Recessive Lethals in Natural Populations of Bluefin Killifish and Zebrafish , 2002, Science.