Lines of Danio rerio selected for opposite behavioural lateralization show differences in anatomical left–right asymmetries

Previous studies suggest that laterality of the viscera, morphological asymmetries of the brain, and lateralization of cognitive functions have a common genetic origin. To test this hypothesis, we conducted an artificial selection experiment for behavioural lateralization of eye use in two strains (TL and GT) of zebrafish (Danio rerio), maintaining one selected line in each strain for five generations. In addition, we investigated, using molecular markers, whether there was any correlation among directionality in eye preference, diencephalic left-right asymmetries in the brain and positioning of the viscera. After one generation of selection, the right- and left-eye lines of both strains showed a significant difference in the behavioural trait. This difference was maintained for all the five generations even though we observed a progressive decline in the response to artificial selection in subsequent generations for both strains. Overall, anatomical evidence suggests that selection for right-eye use significantly increased the frequency of reversed asymmetry in the epithalamus while selection for left-eye use decreased it. However, the response was irregular since not all samples conformed to this pattern. The association between the direction of behavioural selection and pancreas position was less clear-cut, although the concordance between visceral and brain asymmetries exceeded 90% in both strains.

[1]  Stephen W. Wilson,et al.  Laterotopic Representation of Left-Right Information onto the Dorso-Ventral Axis of a Zebrafish Midbrain Target Nucleus , 2005, Current Biology.

[2]  Giorgio Vallortigara,et al.  Heritability of lateralization in fish: concordance of right–left asymmetry between parents and offspring , 2000, Neuropsychologia.

[3]  R. Collins On the inheritance of handedness. II. Selection for sinistrality in mice. , 1969, The Journal of heredity.

[4]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[5]  Á. Miklósi,et al.  Right eye use associated with decision to bite in zebrafish , 1999, Behavioural Brain Research.

[6]  Stephen W. Wilson,et al.  Asymmetry in the epithalamus of vertebrates , 2001, Journal of anatomy.

[7]  Á. Miklósi,et al.  Behavioural Lateralisation of the Tetrapod Type in the Zebrafish (Brachydanio Rerio) , 1997, Physiology & Behavior.

[8]  R. Collins Reimpressed selective breeding for lateralization of handedness in mice , 1991, Brain Research.

[9]  Y. Kuan,et al.  Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target , 2005, Development.

[10]  K. Kidd,et al.  Hand usage in a colony of bonnett monkeys,Macaca radiata , 1981, Behavior genetics.

[11]  W. Hopkins Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates , 2004, International Journal of Primatology.

[12]  Victoria A. Braithwaite,et al.  Size matters: a test of boldness in eight populations of the poeciliid Brachyraphis episcopi , 2004, Animal Behaviour.

[13]  Luigia Cristino,et al.  The interplay between the pineal complex and the habenular nuclei in lower vertebrates in the context of the evolution of cerebral asymmetry , 2006, Brain Research Bulletin.

[14]  F. Argenton,et al.  Early appearance of pancreatic hormone-expressing cells in the zebrafish embryo , 1999, Mechanisms of Development.

[15]  B. A. Eales,et al.  Genetic variation in paw preference (handedness) in the mouse. , 1993, Genome.

[16]  William D. Hopkins,et al.  Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry , 2008, NeuroImage.

[17]  J. Jaffe,et al.  Handedness in the NAS/NRC twin study. , 1999, Laterality.

[18]  I. Mcmanus,et al.  Right hand, left hand: The origins of asymmetry in brains, bodies, atoms and cultures , 2002 .

[19]  O. Güntürkün,et al.  A morphological study of the nucleus subpretectalis of the pigeon , 2008, Brain Research Bulletin.

[20]  G. Vallortigara,et al.  Lateralization of detour behaviour in poeciliid fish: The effect of species, gender and sexual motivation , 1998, Behavioural Brain Research.

[21]  Stephen W. Wilson,et al.  A Nodal Signaling Pathway Regulates the Laterality of Neuroanatomical Asymmetries in the Zebrafish Forebrain , 2000, Neuron.

[22]  M. Nosten-Bertrand,et al.  Paw preference and intra-/infrapyramidal mossy fibers in the hippocampus of the mouse , 1996, Behavior genetics.

[23]  C. Cantalupo,et al.  Further evidence for mirror-reversed laterality in lines of fish selected for leftward or rightward turning when facing a predator model , 2005, Behavioural Brain Research.

[24]  Stephen W. Wilson,et al.  Local Tissue Interactions across the Dorsal Midline of the Forebrain Establish CNS Laterality , 2003, Neuron.

[25]  B. A. Eales,et al.  The degree of lateralization of paw usage (handedness) in the mouse is defined by three major phenotypes , 1996, Behavior genetics.

[26]  J. Postlethwait,et al.  Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. , 1993, Development.

[27]  G. Vallortigara,et al.  Consistency among different tasks of left–right asymmetries in lines of fish originally selected for opposite direction of lateralization in a detour task , 2001, Neuropsychologia.

[28]  Giorgio Vallortigara,et al.  What causes lateralization of detour behavior in fish? evidence for asymmetries in eye use , 1999, Behavioural Brain Research.

[29]  Á. Miklósi,et al.  Early asymmetries in the behaviour of zebrafish larvae , 2004, Behavioural Brain Research.

[30]  K M O'Craven,et al.  Structural and functional brain asymmetries in human situs inversus totalis , 1999, Neurology.

[31]  H. Yost,et al.  Multiple pathways in the midline regulate concordant brain, heart and gut left-right asymmetry. , 2000, Development.

[32]  M. Hori,et al.  Frequency-Dependent Natural Selection in the Handedness of Scale-Eating Cichlid Fish , 1993, Science.

[33]  M. Dadda,et al.  Artificial selection on laterality in the teleost fish Girardinus falcatus , 2007, Behavioural Brain Research.

[34]  V. Denenberg,et al.  A measure of lateral paw preference in the mouse , 1991, Physiology & Behavior.

[35]  Robert L. Collins,et al.  Structural asymmetries in brains of mice selected for strong lateralization , 1984, Brain Research.

[36]  M. Lassonde,et al.  The relationship between callosal variation and lateralization in mice is genotype-dependent , 1987, Brain Research.

[37]  Lesley J. Rogers,et al.  Comparative Vertebrate Lateralization , 2008 .

[38]  Omid B. Rahimi,et al.  Distinct patterns of gene expression in the left and right hippocampal formation of developing rats , 2006, Hippocampus.

[39]  V. Denenberg,et al.  Analysis of two measures of paw preference in a large population of inbred mice , 1994, Behavioural Brain Research.

[40]  Á. Miklósi,et al.  Role of right hemifield in visual control of approach to target in zebrafish , 2001, Behavioural Brain Research.

[41]  R. Collins,et al.  On the inheritance of handedness. I. Laterality in inbred mice. , 1968, The Journal of heredity.

[42]  R. Collins 3 – On the Inheritance of Direction and Degree of Asymmetry , 1985 .

[43]  G. Vallortigara,et al.  Detour tests reveal task- and stimulus-specific behavioural lateralization in mosquitofish (Gambusia holbrooki) , 1997, Behavioural Brain Research.

[44]  J. F. Dahl,et al.  Genetic Influence on the Expression of Hand Preferences in Chimpanzees (Pan Troglodytes): Evidence in Support of the Right-Shift Theory and Developmental Instability , 2001, Psychological science.

[45]  M. Halpern,et al.  Leaning to the left: laterality in the zebrafish forebrain , 2003, Trends in Neurosciences.

[46]  H. Yost,et al.  Molecular mechanisms of vertebrate left-right development. , 1998, Trends in genetics : TIG.

[47]  M. Halpern,et al.  The parapineal mediates left-right asymmetry in the zebrafish diencephalon , 2003, Development.

[48]  W. Hopkins,et al.  Heritability of hand preference in chimpanzees (Pan). , 1994, The International journal of neuroscience.

[49]  I. Mcmanus,et al.  Handedness in twins: A critical review , 1980, Neuropsychologia.

[50]  Stephen W. Wilson,et al.  fsi Zebrafish Show Concordant Reversal of Laterality of Viscera, Neuroanatomy, and a Subset of Behavioral Responses , 2005, Current Biology.

[51]  H. Yost Left-right development in Xenopus and zebrafish. , 1998, Seminars in cell & developmental biology.

[52]  M. Corballis The genetics and evolution of handedness. , 1997, Psychological review.

[53]  M. Sugishita,et al.  Dichotic listening in patients with situs inversus:brain asymmetry and situs asymmetry , 1999, Neuropsychologia.

[54]  R. Andrew,et al.  Eye use during viewing a reflection: Behavioural lateralisation in zebrafish larvae , 2006, Behavioural Brain Research.

[55]  Kunio Watanabe,et al.  Lateralized Hand Use in the Precultural Behavior of the Koshima Monkeys (Macaca fuscata) , 1993 .