Thermal experience during embryogenesis contributes to the induction of dwarfism in whitefish Coregonus lavaretus
Ecotype pairs provide well-suited model systems for study of intraspecific phenotypical diversification of animals. However, little is still known about the processes that account for the development of different forms and sizes within a species, particularly in teleosts. Here, embryos of a normal-g...
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description | Ecotype pairs provide well-suited model systems for study of intraspecific phenotypical diversification of animals. However, little is still known about the processes that account for the development of different forms and sizes within a species, particularly in teleosts. Here, embryos of a normal-growing 'large' form and a dwarf form of whitefish Coregonus lavaretus were incubated at two temperatures that are usually experienced at their own spawning sites (2°C for the normal and 6°C for the dwarf form). All fish were subjected to similar thermal treatment after hatching. The present data demonstrate for the first time that different thermal experience in embryonic life has lasting effects on body and muscle growth of this ecotype pair and contributes to the development of the dwarf form. Thus, juvenile fish of the regular form are much smaller and have less muscle mass when pre-hatching thermal conditions were similar to those typical for the spawning sites of the dwarf form (6°C) than when subjected to conditions of their own spawning sites (2°C). Surprisingly, fish of the dwarf form exhibit a similar pattern of response to thermal history (2°-fish much larger than 6°-fish), indicating that in their case, normal spawning site temperature (6°C) is indeed likely to act as a growth limiting factor. Results also demonstrate that the hypertrophic and hyperplastic muscle growth modes are similarly affected by thermal history. Immunolabelling experiments for Pax7, H3P and Mef2 provide evidence that the cellular mechanisms behind the increased growth rates after cold incubation in both ecotypes are increased proliferation and reduced differentiation rates of muscle precursor cells. This is of major significance to aspects of ecological and developmental biology and from the evolutionary perspective. |
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However, little is still known about the processes that account for the development of different forms and sizes within a species, particularly in teleosts. Here, embryos of a normal-growing 'large' form and a dwarf form of whitefish Coregonus lavaretus were incubated at two temperatures that are usually experienced at their own spawning sites (2°C for the normal and 6°C for the dwarf form). All fish were subjected to similar thermal treatment after hatching. The present data demonstrate for the first time that different thermal experience in embryonic life has lasting effects on body and muscle growth of this ecotype pair and contributes to the development of the dwarf form. Thus, juvenile fish of the regular form are much smaller and have less muscle mass when pre-hatching thermal conditions were similar to those typical for the spawning sites of the dwarf form (6°C) than when subjected to conditions of their own spawning sites (2°C). Surprisingly, fish of the dwarf form exhibit a similar pattern of response to thermal history (2°-fish much larger than 6°-fish), indicating that in their case, normal spawning site temperature (6°C) is indeed likely to act as a growth limiting factor. Results also demonstrate that the hypertrophic and hyperplastic muscle growth modes are similarly affected by thermal history. Immunolabelling experiments for Pax7, H3P and Mef2 provide evidence that the cellular mechanisms behind the increased growth rates after cold incubation in both ecotypes are increased proliferation and reduced differentiation rates of muscle precursor cells. This is of major significance to aspects of ecological and developmental biology and from the evolutionary perspective.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0185384</identifier><identifier>PMID: 28945823</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animals ; Biological evolution ; Biology ; Biology and Life Sciences ; Body Size - physiology ; Cell proliferation ; Developmental biology ; Differentiation ; Diversification ; Dwarfism ; Dwarfism - embryology ; Dwarfism - physiopathology ; Dwarfism - veterinary ; Earth Sciences ; Ecology and Environmental Sciences ; Ecotypes ; Embryogenesis ; Embryonic development ; Embryonic Development - physiology ; Embryonic growth stage ; Embryos ; Environmental aspects ; Eutrophication ; Factorial experiments ; Fish ; Fish Diseases - embryology ; Fish Diseases - pathology ; Fish Diseases - physiopathology ; Genetic aspects ; Hatching ; Heat treatment ; Incubation ; Lake whitefish ; Lakes ; Medicine and Health Sciences ; Muscle Fibers, Fast-Twitch - cytology ; Muscle Fibers, Fast-Twitch - physiology ; Muscle, Skeletal - embryology ; Muscle, Skeletal - growth & development ; Muscle, Skeletal - physiology ; Myoblasts, Skeletal - cytology ; Myoblasts, Skeletal - physiology ; Physiological aspects ; Physiology ; Risk factors ; Salmon ; Salmonidae - embryology ; Salmonidae - growth & development ; Salmonidae - physiology ; Spawning ; Studies ; Temperature ; Temperature effects ; Zebrafish</subject><ispartof>PloS one, 2017-09, Vol.12 (9), p.e0185384-e0185384</ispartof><rights>COPYRIGHT 2017 Public Library of Science</rights><rights>2017 Steinbacher et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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However, little is still known about the processes that account for the development of different forms and sizes within a species, particularly in teleosts. Here, embryos of a normal-growing 'large' form and a dwarf form of whitefish Coregonus lavaretus were incubated at two temperatures that are usually experienced at their own spawning sites (2°C for the normal and 6°C for the dwarf form). All fish were subjected to similar thermal treatment after hatching. The present data demonstrate for the first time that different thermal experience in embryonic life has lasting effects on body and muscle growth of this ecotype pair and contributes to the development of the dwarf form. Thus, juvenile fish of the regular form are much smaller and have less muscle mass when pre-hatching thermal conditions were similar to those typical for the spawning sites of the dwarf form (6°C) than when subjected to conditions of their own spawning sites (2°C). Surprisingly, fish of the dwarf form exhibit a similar pattern of response to thermal history (2°-fish much larger than 6°-fish), indicating that in their case, normal spawning site temperature (6°C) is indeed likely to act as a growth limiting factor. Results also demonstrate that the hypertrophic and hyperplastic muscle growth modes are similarly affected by thermal history. Immunolabelling experiments for Pax7, H3P and Mef2 provide evidence that the cellular mechanisms behind the increased growth rates after cold incubation in both ecotypes are increased proliferation and reduced differentiation rates of muscle precursor cells. 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embryology</subject><subject>Fish Diseases - pathology</subject><subject>Fish Diseases - physiopathology</subject><subject>Genetic aspects</subject><subject>Hatching</subject><subject>Heat treatment</subject><subject>Incubation</subject><subject>Lake whitefish</subject><subject>Lakes</subject><subject>Medicine and Health Sciences</subject><subject>Muscle Fibers, Fast-Twitch - cytology</subject><subject>Muscle Fibers, Fast-Twitch - physiology</subject><subject>Muscle, Skeletal - embryology</subject><subject>Muscle, Skeletal - growth & development</subject><subject>Muscle, Skeletal - physiology</subject><subject>Myoblasts, Skeletal - cytology</subject><subject>Myoblasts, Skeletal - physiology</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Risk factors</subject><subject>Salmon</subject><subject>Salmonidae - embryology</subject><subject>Salmonidae - growth & development</subject><subject>Salmonidae - physiology</subject><subject>Spawning</subject><subject>Studies</subject><subject>Temperature</subject><subject>Temperature effects</subject><subject>Zebrafish</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk0lr3DAUx01padK036C0gkJpDzOVtXi5BMLQZSAQaNNehWw92xpsaSLJWb595YwTZkoORQdJT7_3l_SWJHmb4mVK8_TLxo7OyH65tQaWOC04Ldiz5DgtKVlkBNPne-uj5JX3G4wjk2UvkyNSlIwXhB4nV5cduEH2CG634DSYGpAanTYtgqFyd7YFA157VFsTnK7GAB4Fi0IHSBs11kFbg2yD1I10jfZDtKKbTgeImw6trIPWmtGjXl5LB2H0r5MXjew9vJnnk-T3t6-Xqx-L84vv69XZ-aLOShIWEqRUXGWgcFNyUgFlBWkow3VRSUV5jklV8SrLc4wbKBrVNLhQUIGSpCRQ0JPk_U5321sv5mh5kZaMZGmZEx6J9Y5QVm7E1ulBujthpRb3ButaIV3QdQ9CAmYKaJ1zRllZMSnThnHFCuAcl5JGrdP5trEaQNUQoyX7A9HDE6M70dprwbOU5Hx6zKdZwNmrEXwQg_Y19L00YMf7d1NSMJ7mEf3wD_r072aqlfED2jQ23ltPouKM44zRPFZRpJZPUHEoGHTMeUxjtB84fD5wmOoCbkMrR-_F-tfP_2cv_hyyH_fYDmQfOm_7caovfwiyHVg7672D5jHIKRZTZzxEQ0ydIebOiG7v9hP06PTQCvQv0sEMRg</recordid><startdate>20170925</startdate><enddate>20170925</enddate><creator>Steinbacher, Peter</creator><creator>Wanzenböck, Josef</creator><creator>Brandauer, Magdalena</creator><creator>Holper, Raphael</creator><creator>Landertshammer, Jasmin</creator><creator>Mayr, Magdalena</creator><creator>Platzl, Christian</creator><creator>Stoiber, Walter</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-8033-5190</orcidid></search><sort><creationdate>20170925</creationdate><title>Thermal experience during embryogenesis contributes to the induction of dwarfism in whitefish Coregonus lavaretus</title><author>Steinbacher, Peter ; Wanzenböck, Josef ; Brandauer, Magdalena ; Holper, Raphael ; Landertshammer, Jasmin ; Mayr, Magdalena ; Platzl, Christian ; Stoiber, Walter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-aeaad5d6ed0f952be3482f340c8bad35702bb5b67700fe8fdff08debeda292e83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Analysis</topic><topic>Animals</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Biology and Life Sciences</topic><topic>Body Size - 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However, little is still known about the processes that account for the development of different forms and sizes within a species, particularly in teleosts. Here, embryos of a normal-growing 'large' form and a dwarf form of whitefish Coregonus lavaretus were incubated at two temperatures that are usually experienced at their own spawning sites (2°C for the normal and 6°C for the dwarf form). All fish were subjected to similar thermal treatment after hatching. The present data demonstrate for the first time that different thermal experience in embryonic life has lasting effects on body and muscle growth of this ecotype pair and contributes to the development of the dwarf form. Thus, juvenile fish of the regular form are much smaller and have less muscle mass when pre-hatching thermal conditions were similar to those typical for the spawning sites of the dwarf form (6°C) than when subjected to conditions of their own spawning sites (2°C). Surprisingly, fish of the dwarf form exhibit a similar pattern of response to thermal history (2°-fish much larger than 6°-fish), indicating that in their case, normal spawning site temperature (6°C) is indeed likely to act as a growth limiting factor. Results also demonstrate that the hypertrophic and hyperplastic muscle growth modes are similarly affected by thermal history. Immunolabelling experiments for Pax7, H3P and Mef2 provide evidence that the cellular mechanisms behind the increased growth rates after cold incubation in both ecotypes are increased proliferation and reduced differentiation rates of muscle precursor cells. 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recordid | cdi_plos_journals_1942619725 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
subjects | Analysis Animals Biological evolution Biology Biology and Life Sciences Body Size - physiology Cell proliferation Developmental biology Differentiation Diversification Dwarfism Dwarfism - embryology Dwarfism - physiopathology Dwarfism - veterinary Earth Sciences Ecology and Environmental Sciences Ecotypes Embryogenesis Embryonic development Embryonic Development - physiology Embryonic growth stage Embryos Environmental aspects Eutrophication Factorial experiments Fish Fish Diseases - embryology Fish Diseases - pathology Fish Diseases - physiopathology Genetic aspects Hatching Heat treatment Incubation Lake whitefish Lakes Medicine and Health Sciences Muscle Fibers, Fast-Twitch - cytology Muscle Fibers, Fast-Twitch - physiology Muscle, Skeletal - embryology Muscle, Skeletal - growth & development Muscle, Skeletal - physiology Myoblasts, Skeletal - cytology Myoblasts, Skeletal - physiology Physiological aspects Physiology Risk factors Salmon Salmonidae - embryology Salmonidae - growth & development Salmonidae - physiology Spawning Studies Temperature Temperature effects Zebrafish |
title | Thermal experience during embryogenesis contributes to the induction of dwarfism in whitefish Coregonus lavaretus |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-01T21%3A14%3A09IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Thermal%20experience%20during%20embryogenesis%20contributes%20to%20the%20induction%20of%20dwarfism%20in%20whitefish%20Coregonus%20lavaretus&rft.jtitle=PloS%20one&rft.au=Steinbacher,%20Peter&rft.date=2017-09-25&rft.volume=12&rft.issue=9&rft.spage=e0185384&rft.epage=e0185384&rft.pages=e0185384-e0185384&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0185384&rft_dat=%3Cgale_plos_%3EA506437371%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1942619725&rft_id=info:pmid/28945823&rft_galeid=A506437371&rft_doaj_id=oai_doaj_org_article_ae04de3c754349b4aa1f45d48e5509a3&rfr_iscdi=true |