Sexual Dimorphism of the Zebra Finch Syrinx Indicates Adaptation for High Fundamental Frequencies in Males
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{"title"=>"Sexual dimorphism of the zebra finch syrinx indicates adaptation for high fundamental frequencies in males", "type"=>"journal", "authors"=>[{"first_name"=>"Tobias", "last_name"=>"Riede", "scopus_author_id"=>"6701515719"}, {"first_name"=>"John H.", "last_name"=>"Fisher", "scopus_author_id"=>"36449739200"}, {"first_name"=>"Franz", "last_name"=>"Goller", "scopus_author_id"=>"7003726792"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"359306478", "doi"=>"10.1371/journal.pone.0011368", "sgr"=>"77955322950", "isbn"=>"1932-6203 (Electronic)\r1932-6203 (Linking)", "pmid"=>"20614010", "scopus"=>"2-s2.0-77955322950"}, "id"=>"47ee4bc9-f86c-3af5-a72f-e5ba71afce26", "abstract"=>"BACKGROUND: In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.\\n\\nCONCLUSIONS/SIGNIFICANCE: The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.", "link"=>"http://www.mendeley.com/research/sexual-dimorphism-zebra-finch-syrinx-indicates-adaptation-high-fundamental-frequencies-males", "reader_count"=>37, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>5, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Environmental Science"=>1, "Agricultural and Biological Sciences"=>27, "Neuroscience"=>5, "Physics and Astronomy"=>1, "Psychology"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>5}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>2, "Germany"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/842704"], "description"=>"<p>Fundamental frequency and air sac pressure was also measured in the respiratory sounds (“rs”). ‘High’ and ‘Low’ fundamental frequency (F0) in male calls (“highF0” and “lowF0”) is explained in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone-0011368-g002\" target=\"_blank\">Figure 2</a>. Means were calculated from individual means (number of individuals, N, indicated in each category) which are based on measurements in twenty calls. The probability levels that the slopes are greater than zero is P = 0.006 before and P = 0.012 after the nervecut.</p>", "links"=>[], "tags"=>["sac", "calls", "bilateral", "neurotomy"], "article_id"=>513152, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011368.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fundamental_frequency_and_air_sac_pressure_measurements_mean_177_1_standard_deviation_in_female_and_male_calls_before_8220_pre_8221_and_after_bilateral_neurotomy_8220_post_8221_/513152", "title"=>"Fundamental frequency and air sac pressure measurements (mean ±1 standard deviation) in female and male calls before (“pre”) and after bilateral neurotomy (“post”).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:52:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/842484"], "description"=>"<p><b>A–E</b> illustrate active, muscular and passive, pressure-driven control of the syringeal valve (corresponding to “active and passive closure models” of Gaunt, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Gaunt1\" target=\"_blank\">[22]</a>). Stained sections of a female (<b>F</b>) and male (<b>G</b>) syrinx at about mid organ level illustrate sexual dimorphism in muscle mass and bronchial half rings. Syringeal muscles adjust the position of the labia and therefore adjust the valve from complete closure to active opening. A partially adducted position is also assumed for induction of phonation <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Mindlin1\" target=\"_blank\">[23]</a>. <b>A.</b> Neutral position of labia. <b>B.</b> Rotation of the third bronchial half ring moves the lateral labium into the bronchial lumen <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Miskimen1\" target=\"_blank\">[24]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Chamberlain1\" target=\"_blank\">[25]</a>. <b>C.</b> The first and second bronchial half rings arch with their end points into the ventral and the dorsal aspect of the medial labium and therefore tense the labial tissue but also exert control over its position <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Riede2\" target=\"_blank\">[9]</a>. The valve control mechanisms in <b>B</b> and <b>C</b> most likely occur simultaneously, but are effected by different syringeal muscles. The dorsal and ventral tracheobronchial muscles act as adductor and abductor of the lateral labium, respectively <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Goller2\" target=\"_blank\">[26]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Goller3\" target=\"_blank\">[27]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Larsen1\" target=\"_blank\">[28]</a>. The role of the ventral syringeal muscle appears to include abductive activity, as indicated by its activation during the expiratory phase during quiet respiration <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Goller1\" target=\"_blank\">[6]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Vicario1\" target=\"_blank\">[29]</a>. <b>D</b> and <b>E.</b> A second mechanism for adjusting labial position is passive. The syrinx is located inside the interclavicular air sac (ICAS). Pressure variation inside the subsyringeal air sac system causes similar pressure variation in the ICAS. The medial labium therefore passively moves into or out of the bronchial lumen if there is a pressure differential between the bronchial lumen (P<sub>L</sub>) and the ICAS (P<sub>I</sub>) (first described by Hérissant in 1753, after Gaunt <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Gaunt1\" target=\"_blank\">[22]</a>). ICAS pressure is larger than pressure in the bronchial lumen during expiration and smaller during inspiration. Muscle activity synchronized with the respiratory cycle <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Goller1\" target=\"_blank\">[6]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Vicario1\" target=\"_blank\">[29]</a> keeps the syringeal lumen open during expiration. Without muscle activity the lumen closes during expiration (<b>D</b>) and opens during inspiration (<b>E</b>). During expiration, the medial and lateral labia are sufficiently adducted that increased flow causes self-sustained oscillations of the labia and, thus, generates sound. Phonation is maintained as long as an asymmetric shape of the labia is combined with flow separation right behind the labia as long as the driving pressure is high enough <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011368#pone.0011368-Mindlin1\" target=\"_blank\">[23]</a>. Abbreviations: P, pessulus; A1, A2, A3, three bronchial half rings; ML, Medial labium, MTM, Medial tympaniform membrane, LL, Lateral labium, Tr, tracheal ring; D, drum; M, intrinsic syringeal muscles; B, bronchial ring; arrows in <b>C</b> and <b>E</b> indicate air flow direction. The bar in <b>G</b> indicates a 1 mm distance and applied to <b>F</b> and <b>G</b>.</p>", "links"=>[], "tags"=>["stained", "frontal", "sections"], "article_id"=>512935, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011368.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_and_H_amp_E_stained_frontal_sections_through_the_syrinx_/512935", "title"=>"Schematic and H&E stained frontal sections through the syrinx.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:48:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/842617"], "description"=>"<p>The two arrows in <b>A</b> indicate a high (1) fundamental frequency at the beginning of the male call and a low (2) fundamental frequency in the middle and end of a male distance call. This frequency modulation does not occur in females and was also missing in one of the three males in this study. Calls in <b>A</b> and <b>B</b> are representative before nervecut surgery, and <b>C</b> and <b>D</b> are examples from the same individuals after tracheosyringeal nervecut.</p>", "links"=>[], "tags"=>["spectrogram", "subsyringeal", "sac", "examples", "respiratory", "sounds"], "article_id"=>513064, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011368.g002", "stats"=>{"downloads"=>2, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Oscillogram_top_panel_spectrogram_middle_panel_and_subsyringeal_air_sac_pressure_bottom_panel_of_a_male_A_before_nerve_cut_C_same_individual_after_nervecut_and_a_female_B_before_nerve_cut_D_same_individual_after_nervecut_distance_call_as_well_as_of_two_r/513064", "title"=>"Oscillogram (top panel), spectrogram (middle panel) and subsyringeal air sac pressure (bottom panel) of a male (A, before nerve cut, C, same individual after nervecut) and a female (B, before nerve cut, D, same individual after nervecut) distance call as well as of two representative examples of respiratory sounds (E).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:51:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/420128", "https://ndownloader.figshare.com/files/420180", "https://ndownloader.figshare.com/files/420209", "https://ndownloader.figshare.com/files/420226", "https://ndownloader.figshare.com/files/420243", "https://ndownloader.figshare.com/files/420265", "https://ndownloader.figshare.com/files/420282"], "description"=>"<div><h3>Background</h3><p>In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.</p><h3>Methodology/Principal Findings</h3><p>Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.</p><h3>Conclusions/Significance</h3><p>The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.</p></div>", "links"=>[], "tags"=>["dimorphism", "zebra", "finch", "syrinx", "indicates", "adaptation", "frequencies", "males"], "article_id"=>142947, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011368.s001", "https://dx.doi.org/10.1371/journal.pone.0011368.s002", "https://dx.doi.org/10.1371/journal.pone.0011368.s003", "https://dx.doi.org/10.1371/journal.pone.0011368.s004", "https://dx.doi.org/10.1371/journal.pone.0011368.s005", "https://dx.doi.org/10.1371/journal.pone.0011368.s006", "https://dx.doi.org/10.1371/journal.pone.0011368.s007"], "stats"=>{"downloads"=>7, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Sexual_Dimorphism_of_the_Zebra_Finch_Syrinx_Indicates_Adaptation_for_High_Fundamental_Frequencies_in_Males/142947", "title"=>"Sexual Dimorphism of the Zebra Finch Syrinx Indicates Adaptation for High Fundamental Frequencies in Males", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-06-29 00:49:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/842773"], "description"=>"<p>Before nervecut (full symbols); after nervecut (open symbols). Respiratory sounds in males (+) and females (-) are only present after the nervecut. The regression lines were calculated using all pre-neurotomy data (solid line) and all post-neurotomy data (dashed line). The arrows on the side indicate fundamental frequency ranges which are regulated by abdominal pressure or by a combination of abdominal pressure and muscle activity. Pressure and muscle regulated range extends up to 4 kHz for some song syllables. Pressure in those high frequency song syllables does not exceed 5 kPa (data not presented here).</p>", "links"=>[], "tags"=>["subsyringeal", "sac"], "article_id"=>513230, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011368.g004", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_fundamental_frequency_and_subsyringeal_air_sac_pressure_/513230", "title"=>"Relationship between fundamental frequency and subsyringeal air sac pressure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:53:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/842857"], "description"=>"<p>Average data, coefficients of variation (CV) and t-tests comparing males and females for 18 measurements.</p>", "links"=>[], "tags"=>["coefficients", "t-tests", "comparing", "males", "females", "18"], "article_id"=>513308, "categories"=>["Physiology", "Neuroscience"], "users"=>["Tobias Riede", "John H. Fisher", "Franz Goller"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011368.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Average_data_coefficients_of_variation_CV_and_t_tests_comparing_males_and_females_for_18_measurements_/513308", "title"=>"Average data, coefficients of variation (CV) and t-tests comparing males and females for 18 measurements.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-29 00:55:08"}

PMC Usage Stats | Further Information

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