Heritable Differences in Schooling Behavior among Threespine Stickleback Populations Revealed by a Novel Assay
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{"title"=>"Heritable differences in schooling behavior among threespine stickleback populations revealed by a novel assay", "type"=>"journal", "authors"=>[{"first_name"=>"Abigail R.", "last_name"=>"Wark", "scopus_author_id"=>"24778835900"}, {"first_name"=>"Anna K.", "last_name"=>"Greenwood", "scopus_author_id"=>"8604144200"}, {"first_name"=>"Elspeth M.", "last_name"=>"Taylor", "scopus_author_id"=>"37096257600"}, {"first_name"=>"Kohta", "last_name"=>"Yoshida", "scopus_author_id"=>"55634256800"}, {"first_name"=>"Catherine L.", "last_name"=>"Peichel", "scopus_author_id"=>"6602163057"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-79953054281", "sgr"=>"79953054281", "pui"=>"361500746", "isbn"=>"1932-6203", "pmid"=>"21464914", "doi"=>"10.1371/journal.pone.0018316"}, "id"=>"ef199d3d-e2f1-380c-9957-d66fa576d0b4", "abstract"=>"Identifying the proximate and ultimate mechanisms of social behavior remains a major goal of behavioral biology. In particular, the complex social interactions mediating schooling behavior have long fascinated biologists, leading to theoretical and empirical investigations that have focused on schooling as a group-level phenomenon. However, methods to examine the behavior of individual fish within a school are needed in order to investigate the mechanisms that underlie both the performance and the evolution of schooling behavior. We have developed a technique to quantify the schooling behavior of an individual in standardized but easily manipulated social circumstances. Using our model school assay, we show that threespine sticklebacks (Gasterosteus aculeatus) from alternative habitats differ in behavior when tested in identical social circumstances. Not only do marine sticklebacks show increased association with the model school relative to freshwater benthic sticklebacks, they also display a greater degree of parallel swimming with the models. Taken together, these data indicate that marine sticklebacks exhibit a stronger tendency to school than benthic sticklebacks. We demonstrate that these population-level differences in schooling tendency are heritable and are shared by individuals within a population even when they have experienced mixed-population housing conditions. Finally, we begin to explore the stimuli that elicit schooling behavior in these populations. Our data suggest that the difference in schooling tendency between marine and benthic sticklebacks is accompanied by differential preferences for social vs. non-social and moving vs. stationary shelter options. Our study thus provides novel insights into the evolution of schooling behavior, as well as a new experimental approach to investigate the genetic and neural mechanisms that underlie this complex social behavior.", "link"=>"http://www.mendeley.com/research/heritable-differences-schooling-behavior-among-threespine-stickleback-populations-revealed-novel-ass", "reader_count"=>83, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>28, "Student > Master"=>16, "Other"=>1, "Student > Bachelor"=>8, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>28, "Student > Master"=>16, "Other"=>1, "Student > Bachelor"=>8, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>2, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Engineering"=>1, "Environmental Science"=>6, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>62, "Neuroscience"=>1, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>1, "Earth and Planetary Sciences"=>1, "Sports and Recreations"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Neuroscience"=>{"Neuroscience"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>62}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>6}}, "reader_count_by_country"=>{"Romania"=>1, "United States"=>5, "Philippines"=>1, "United Kingdom"=>2, "South Africa"=>1, "Portugal"=>3, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/788259"], "description"=>"<p>(A) Twelve individual marine (left column) and benthic (right column) sticklebacks were tracked for 40 seconds in free-swimming groups within a circular tank (indicated by the area in white). Panels show consecutive 10-second increments. Each colored path represents a single individual, and each point represents the position of the individual at a one-second interval. Large circles mark the final position for each time bin and therefore indicate swimming direction. (B) Cumulative tracks for marine (top panel) and benthic (bottom panel) sticklebacks for the entire 40 seconds.</p>", "links"=>[], "tags"=>["schooling", "differs", "benthic"], "article_id"=>458631, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spontaneous_schooling_behavior_differs_between_marine_and_benthic_sticklebacks_/458631", "title"=>"Spontaneous schooling behavior differs between marine and benthic sticklebacks.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-25 02:23:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/788351"], "description"=>"<p>(A) Schematic depicting mixed species tournament schooling assay. Six marine and six benthic sticklebacks were placed in a large tank, and all schooling fish were caught in a net. School composition was noted, and schooling fish were marked. Fish were retested two more times, for a total of three rounds. Three independent groups of twelve fish were tested. (B) Marine sticklebacks were found in the school significantly more often than benthic sticklebacks. The mean number of fish (± SEM) from each population that schooled at least once during the assay is shown. <i>n</i> = 3 groups of six fish for marine (black bars) and benthic (red bars).</p>", "links"=>[], "tags"=>["sticklebacks", "benthic"], "article_id"=>458722, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Marine_sticklebacks_school_more_than_benthic_sticklebacks_in_mixed_population_schools_/458722", "title"=>"Marine sticklebacks school more than benthic sticklebacks in mixed population schools.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-25 02:25:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/788525"], "description"=>"<p>(A,E) Schematic diagrams showing assays used for testing preference for the model school or plant stimuli using either (A) moving (marine: <i>n</i> = 10, benthic: <i>n</i> = 10) or (E) stationary plant (marine: <i>n</i> = 9, benthic: <i>n</i> = 9) choices. (B,C,D) results from moving plant trials and (F,G,H) results from stationary plant trials. (B,F) time spent with school or plant; (C,G) number of approaches to school or plant; (D,H) latency to approach school or plant. Black symbols and lines represent marines; red represent benthics. A dashed line indicates a significant pairwise comparison between plant and school for a single population. An asterisk indicates a significant pairwise comparison between benthic and marine for a single stimulus.</p>", "links"=>[], "tags"=>["benthic", "sticklebacks", "preferences", "non-social"], "article_id"=>458894, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316.g005", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Marine_and_benthic_sticklebacks_display_different_preferences_for_social_and_non_social_stimuli_/458894", "title"=>"Marine and benthic sticklebacks display different preferences for social and non-social stimuli.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-25 02:28:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/788407"], "description"=>"<p>(A) Schooling behavior was tested by presenting experimental fish with a model school made up of eight polyurethane stickleback casts. An external motor rotated a bicycle wheel above the circular testing tank, causing the model school to “swim” around the tank. (D) Example model stickleback (cast from a benthic×marine F2 hybrid) used in the model school assay. Scale bar = 1 cm. (B,C) results from single population housing conditions (marine: <i>n</i> = 19, benthic: <i>n</i> = 20); (E,F) results from mixed population housing conditions (marine: <i>n</i> = 10, benthic: <i>n</i> = 10). (B,E) time spent schooling and (C,F) latency to approach school. All bars represent mean ± SEM. Black bars = marine and red bars = benthic. Asterisks indicate significant comparisons.</p>", "links"=>[], "tags"=>["sticklebacks", "benthic"], "article_id"=>458780, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316.g003", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Marine_sticklebacks_spend_more_time_with_the_model_school_than_benthic_sticklebacks_/458780", "title"=>"Marine sticklebacks spend more time with the model school than benthic sticklebacks.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-25 02:26:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/788469"], "description"=>"<p>(A,B) Silhouettes of schooling marine (A) and benthic (B) sticklebacks traced from video clips during the model school assay. Four frames from each of two fish are shown for each population. These examples were randomly chosen from the subset of frames in which the fish was actively schooling. The position of the model sticklebacks are shown in open silhouettes, test fish are in filled silhouettes. Grey = marine, red = benthic. (C) Summary figure showing the average <i>x</i>- and <i>y</i>-positions and angle of each population during the model school assay. The <i>x</i>- and <i>y</i>-position is shown with a filled circle (black = marine, <i>n</i> = 19; red = benthic, <i>n</i> = 20); error bars represent the standard deviation. The average angle is shown as an angled line, and the standard deviation is represented by a triangle (grey = marine, <i>n</i> = 19; red = benthic, <i>n</i> = 20). See text for statistical tests.</p>", "links"=>[], "tags"=>["benthic", "sticklebacks", "positions"], "article_id"=>458841, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Marine_and_benthic_sticklebacks_assume_different_positions_with_the_model_school_/458841", "title"=>"Marine and benthic sticklebacks assume different positions with the model school.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-03-25 02:27:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/394770"], "description"=>"<div><p>Identifying the proximate and ultimate mechanisms of social behavior remains a major goal of behavioral biology. In particular, the complex social interactions mediating schooling behavior have long fascinated biologists, leading to theoretical and empirical investigations that have focused on schooling as a group-level phenomenon. However, methods to examine the behavior of <em>individual</em> fish within a school are needed in order to investigate the mechanisms that underlie both the performance and the evolution of schooling behavior. We have developed a technique to quantify the schooling behavior of an individual in standardized but easily manipulated social circumstances. Using our model school assay, we show that threespine sticklebacks (<em>Gasterosteus aculeatus</em>) from alternative habitats differ in behavior when tested in identical social circumstances. Not only do marine sticklebacks show increased association with the model school relative to freshwater benthic sticklebacks, they also display a greater degree of parallel swimming with the models. Taken together, these data indicate that marine sticklebacks exhibit a stronger tendency to school than benthic sticklebacks. We demonstrate that these population-level differences in schooling tendency are heritable and are shared by individuals within a population even when they have experienced mixed-population housing conditions. Finally, we begin to explore the stimuli that elicit schooling behavior in these populations. Our data suggest that the difference in schooling tendency between marine and benthic sticklebacks is accompanied by differential preferences for social <em>vs.</em> non-social and moving <em>vs.</em> stationary shelter options. Our study thus provides novel insights into the evolution of schooling behavior, as well as a new experimental approach to investigate the genetic and neural mechanisms that underlie this complex social behavior.</p> </div>", "links"=>[], "tags"=>["heritable", "differences", "schooling", "threespine", "stickleback", "populations", "revealed", "assay"], "article_id"=>137980, "categories"=>["Neuroscience", "Evolutionary Biology"], "users"=>["Abigail R. Wark", "Anna K. Greenwood", "Elspeth M. Taylor", "Kohta Yoshida", "Catherine L. Peichel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0018316", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Heritable_Differences_in_Schooling_Behavior_among_Threespine_Stickleback_Populations_Revealed_by_a_Novel_Assay/137980", "title"=>"Heritable Differences in Schooling Behavior among Threespine Stickleback Populations Revealed by a Novel Assay", "pos_in_sequence"=>0, "defined_type"=>2, "published_date"=>"2011-03-25 02:13:00"}

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Relative Metric

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