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      Genetic Mapping of Natural Variation in Schooling Tendency in the Threespine Stickleback

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          Abstract

          Although there is a heritable basis for many animal behaviors, the genetic architecture of behavioral variation in natural populations remains mostly unknown, particularly in vertebrates. We sought to identify the genetic basis for social affiliation in two populations of threespine sticklebacks ( Gasterosteus aculeatus) that differ in their propensity to school. Marine sticklebacks from Japan school strongly whereas benthic sticklebacks from a lake in Canada are more solitary. Here, we expanded on our previous efforts to identify quantitative trait loci (QTL) for differences in schooling tendency. We tested fish multiple times in two assays that test different aspects of schooling tendency: 1) the model school assay, which presents fish with a school of eight model sticklebacks; and 2) the choice assay, in which fish are given a choice between the model school and a stationary artificial plant. We found low-to-moderate levels of repeatability, ranging from 0.1 to 0.5, in schooling phenotypes. To identify the genomic regions that contribute to differences in schooling tendency, we used QTL mapping in two types of crosses: benthic × marine backcrosses and an F2 intercross. We found two QTL for time spent with the school in the model school assay, and one QTL for number of approaches to the school in the choice assay. These QTL were on three different linkage groups, not previously linked to behavioral differences in sticklebacks. Our results highlight the importance of using multiple crosses and robust behavioral assays to uncover the genetic basis of behavioral variation in natural populations.

          Most cited references35

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          Genes and social behavior.

          What genes and regulatory sequences contribute to the organization and functioning of neural circuits and molecular pathways in the brain that support social behavior? How does social experience interact with information in the genome to modulate brain activity? Here, we address these questions by highlighting progress that has been made in identifying and understanding two key "vectors of influence" that link genes, the brain, and social behavior: (i) Social information alters gene expression in the brain to influence behavior, and (ii) genetic variation influences brain function and social behavior. We also discuss how evolutionary changes in genomic elements influence social behavior and outline prospects for a systems biology of social behavior.
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            A role for a neo-sex chromosome in stickleback speciation

            Sexual antagonism, or conflict between the sexes, has been proposed as a driving force in both sex chromosome turnover and speciation. Although closely related species often have different sex chromosome systems, it is unknown whether sex chromosome turnover contributes to the evolution of reproductive isolation between species. In this study, we show that a newly evolved sex chromosome harbours genes that contribute to speciation in threespine stickleback fish (Gasterosteus aculeatus). We first identified a neo-sex chromosome system found only in one member of a sympatric species pair in Japan. We then performed genetic linkage mapping of male-specific traits important for reproductive isolation between the Japanese species pair. The neo-X chromosome harbours loci for male courtship display traits that contribute to behavioural isolation, while the ancestral X chromosome contains loci for both behavioural isolation and hybrid male sterility. Our work not only provides strong evidence for a large-X effect on reproductive isolation in a vertebrate system, but also provides direct evidence that a young neo-X chromosome contributes to reproductive isolation between closely related species. Our data suggest that sex chromosome turnover might play a greater role in speciation than previously appreciated.
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              Sociogenomics: social life in molecular terms.

              Spectacular progress in molecular biology, genome-sequencing projects and genomics makes this an appropriate time to attempt a comprehensive understanding of the molecular basis of social life. Promising results have already been obtained in identifying genes that influence animal social behaviour and genes that are implicated in social evolution. These findings - derived from an eclectic mix of species that show varying levels of sociality - provide the foundation for the integration of molecular biology, genomics, neuroscience, behavioural biology and evolutionary biology that is necessary for this endeavour.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                25 February 2015
                May 2015
                : 5
                : 5
                : 761-769
                Affiliations
                [* ]Divisions of Basic Sciences and Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109
                []Program in Molecular and Computational Biology, University of Southern California, Los Angeles, California 90089
                Author notes
                [1 ]Corresponding author: Divisions of Basic Sciences and Human Biology, Fred Hutchinson Cancer Research Center, 1100 Fairview Ave N, Mailstop C2-023, Seattle, WA 98109-1024. E-mail: cpeichel@ 123456fhcrc.org
                Author information
                http://orcid.org/0000-0002-7731-8944
                Article
                GGG_016519
                10.1534/g3.114.016519
                4426364
                25717151
                4c8adbb5-b1dc-49ef-8982-ce0ebbea7484
                Copyright © 2015 Greenwood et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License ( http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 23 December 2014
                : 23 February 2015
                Page count
                Pages: 9
                Categories
                Investigations
                Custom metadata
                v1

                Genetics
                social behavior,evolution,fish,quantitative trait locus (qtl),repeatability
                Genetics
                social behavior, evolution, fish, quantitative trait locus (qtl), repeatability

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