Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths
Identifieur interne : 000395 ( Pmc/Corpus ); précédent : 000394; suivant : 000396Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths
Auteurs : Jelle W. F. Reumer ; Clara M. A. Ten Broek ; Frietson GalisSource :
- PeerJ [ 2167-8359 ] ; 2014.
Abstract
The number of cervical vertebrae in mammals is highly conserved at seven. We have shown that changes of this number are selected against due to a coupling with major congenital abnormalities (pleiotropic effects). Here we show that the incidence of abnormal cervical vertebral numbers in Late Pleistocene mammoths from the North Sea is high (33.3%) and approximately 10 times higher than that of extant elephants (3.6%). Abnormal numbers were due to the presence of large cervical ribs on the seventh vertebra, which we deduced from the presence of rib articulation facets on sixth (posterior side) and seventh (anterior side) cervical vertebrae. The incidence of abnormal cervical vertebral numbers in mammoths appears to be much higher than in other mammalian species, apart from exceptional sloths, manatees and dugongs and indicates a vulnerable condition. We argue that the increased incidence of cervical ribs in mammoths is probably caused by inbreeding and adverse conditions that impact early pregnancies in declining populations close to extinction in the Late Pleistocene.
Url:
DOI: 10.7717/peerj.318
PubMed: 24711969
PubMed Central: 3970796
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PMC:3970796Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths</title><author><name sortKey="Reumer, Jelle W F" sort="Reumer, Jelle W F" uniqKey="Reumer J" first="Jelle W. F." last="Reumer">Jelle W. F. Reumer</name><affiliation><nlm:aff id="aff-1"><institution>Natural History Museum</institution>,<addr-line>Rotterdam</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff-2"><institution>Faculty of Geosciences, Utrecht University</institution>,<addr-line>Utrecht</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation></author><author><name sortKey="Ten Broek, Clara M A" sort="Ten Broek, Clara M A" uniqKey="Ten Broek C" first="Clara M. A." last="Ten Broek">Clara M. A. Ten Broek</name><affiliation><nlm:aff id="aff-3"><institution>Naturalis Biodiversity Center, Terrestrial Zoology/Geology</institution>,<addr-line>Leiden</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff-4"><institution>University Antwerp, Evolutionary Ecology Group</institution>,<addr-line>Antwerp</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Galis, Frietson" sort="Galis, Frietson" uniqKey="Galis F" first="Frietson" last="Galis">Frietson Galis</name><affiliation><nlm:aff id="aff-3"><institution>Naturalis Biodiversity Center, Terrestrial Zoology/Geology</institution>,<addr-line>Leiden</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24711969</idno><idno type="pmc">3970796</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3970796</idno><idno type="RBID">PMC:3970796</idno><idno type="doi">10.7717/peerj.318</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000395</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000395</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths</title><author><name sortKey="Reumer, Jelle W F" sort="Reumer, Jelle W F" uniqKey="Reumer J" first="Jelle W. F." last="Reumer">Jelle W. F. Reumer</name><affiliation><nlm:aff id="aff-1"><institution>Natural History Museum</institution>,<addr-line>Rotterdam</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff-2"><institution>Faculty of Geosciences, Utrecht University</institution>,<addr-line>Utrecht</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation></author><author><name sortKey="Ten Broek, Clara M A" sort="Ten Broek, Clara M A" uniqKey="Ten Broek C" first="Clara M. A." last="Ten Broek">Clara M. A. Ten Broek</name><affiliation><nlm:aff id="aff-3"><institution>Naturalis Biodiversity Center, Terrestrial Zoology/Geology</institution>,<addr-line>Leiden</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff-4"><institution>University Antwerp, Evolutionary Ecology Group</institution>,<addr-line>Antwerp</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Galis, Frietson" sort="Galis, Frietson" uniqKey="Galis F" first="Frietson" last="Galis">Frietson Galis</name><affiliation><nlm:aff id="aff-3"><institution>Naturalis Biodiversity Center, Terrestrial Zoology/Geology</institution>,<addr-line>Leiden</addr-line>,<country>The Netherlands</country></nlm:aff></affiliation></author></analytic><series><title level="j">PeerJ</title><idno type="eISSN">2167-8359</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The number of cervical vertebrae in mammals is highly conserved at seven. We have shown that changes of this number are selected against due to a coupling with major congenital abnormalities (pleiotropic effects). Here we show that the incidence of abnormal cervical vertebral numbers in Late Pleistocene mammoths from the North Sea is high (33.3%) and approximately 10 times higher than that of extant elephants (3.6%). Abnormal numbers were due to the presence of large cervical ribs on the seventh vertebra, which we deduced from the presence of rib articulation facets on sixth (posterior side) and seventh (anterior side) cervical vertebrae. The incidence of abnormal cervical vertebral numbers in mammoths appears to be much higher than in other mammalian species, apart from exceptional sloths, manatees and dugongs and indicates a vulnerable condition. We argue that the increased incidence of cervical ribs in mammoths is probably caused by inbreeding and adverse conditions that impact early pregnancies in declining populations close to extinction in the Late Pleistocene.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Barnard, G" uniqKey="Barnard G">G Barnard</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bateson, W" uniqKey="Bateson W">W Bateson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bots, J" uniqKey="Bots J">J Bots</name></author><author><name sortKey="Wijnaendts, Lc" uniqKey="Wijnaendts L">LC Wijnaendts</name></author><author><name sortKey="Delen, S" uniqKey="Delen S">S Delen</name></author><author><name sortKey="Van Dongen, S" uniqKey="Van Dongen S">S Van Dongen</name></author><author><name sortKey="Heikinheimo, K" uniqKey="Heikinheimo K">K Heikinheimo</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PeerJ</journal-id><journal-id journal-id-type="iso-abbrev">PeerJ</journal-id><journal-id journal-id-type="pmc">PeerJ</journal-id><journal-id journal-id-type="publisher-id">PeerJ</journal-id><journal-title-group><journal-title>PeerJ</journal-title></journal-title-group><issn pub-type="epub">2167-8359</issn><publisher><publisher-name>PeerJ Inc.</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24711969</article-id><article-id pub-id-type="pmc">3970796</article-id><article-id pub-id-type="publisher-id">318</article-id><article-id pub-id-type="doi">10.7717/peerj.318</article-id><article-categories><subj-group subj-group-type="heading"><subject>Evolutionary Studies</subject></subj-group><subj-group subj-group-type="heading"><subject>Paleontology</subject></subj-group></article-categories><title-group><article-title>Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths</article-title></title-group><contrib-group><contrib id="author-1" contrib-type="author"><name><surname>Reumer</surname><given-names>Jelle W.F.</given-names></name><xref ref-type="aff" rid="aff-1">1</xref><xref ref-type="aff" rid="aff-2">2</xref></contrib><contrib id="author-2" contrib-type="author"><name><surname>ten Broek</surname><given-names>Clara M.A.</given-names></name><xref ref-type="aff" rid="aff-3">3</xref><xref ref-type="aff" rid="aff-4">4</xref></contrib><contrib id="author-3" contrib-type="author" corresp="yes"><name><surname>Galis</surname><given-names>Frietson</given-names></name><xref ref-type="aff" rid="aff-3">3</xref><email>frietson.galis@naturalis.nl</email></contrib><aff id="aff-1"><label>1</label><institution>Natural History Museum</institution>,<addr-line>Rotterdam</addr-line>,<country>The Netherlands</country></aff><aff id="aff-2"><label>2</label><institution>Faculty of Geosciences, Utrecht University</institution>,<addr-line>Utrecht</addr-line>,<country>The Netherlands</country></aff><aff id="aff-3"><label>3</label><institution>Naturalis Biodiversity Center, Terrestrial Zoology/Geology</institution>,<addr-line>Leiden</addr-line>,<country>The Netherlands</country></aff><aff id="aff-4"><label>4</label><institution>University Antwerp, Evolutionary Ecology Group</institution>,<addr-line>Antwerp</addr-line>,<country>Belgium</country></aff></contrib-group><contrib-group><contrib id="editor-1" contrib-type="editor"><name><surname>Farke</surname><given-names>Andrew</given-names></name></contrib></contrib-group><pub-date pub-type="epub" date-type="pub" iso-8601-date="2014-03-25"><day>25</day><month>3</month><year iso-8601-date="2014">2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>2</volume><elocation-id>e318</elocation-id><history><date date-type="received" iso-8601-date="2014-02-04"><day>4</day><month>2</month><year iso-8601-date="2014">2014</year></date><date date-type="accepted" iso-8601-date="2014-03-03"><day>3</day><month>3</month><year iso-8601-date="2014">2014</year></date></history><permissions><copyright-statement>© 2014 Reumer et al.</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>Reumer et al.</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.</license-p></license></permissions><self-uri xlink:href="https://peerj.com/articles/318"></self-uri><abstract><p>The number of cervical vertebrae in mammals is highly conserved at seven. We have shown that changes of this number are selected against due to a coupling with major congenital abnormalities (pleiotropic effects). Here we show that the incidence of abnormal cervical vertebral numbers in Late Pleistocene mammoths from the North Sea is high (33.3%) and approximately 10 times higher than that of extant elephants (3.6%). Abnormal numbers were due to the presence of large cervical ribs on the seventh vertebra, which we deduced from the presence of rib articulation facets on sixth (posterior side) and seventh (anterior side) cervical vertebrae. The incidence of abnormal cervical vertebral numbers in mammoths appears to be much higher than in other mammalian species, apart from exceptional sloths, manatees and dugongs and indicates a vulnerable condition. We argue that the increased incidence of cervical ribs in mammoths is probably caused by inbreeding and adverse conditions that impact early pregnancies in declining populations close to extinction in the Late Pleistocene.</p></abstract><kwd-group kwd-group-type="author"><kwd>Mammoths</kwd><kwd>Extinction</kwd><kwd><italic>Loxodonta</italic></kwd><kwd><italic>Elephas</italic></kwd><kwd>Vertebral column</kwd><kwd>Body plan</kwd><kwd>Inbreeding</kwd></kwd-group><funding-group><award-group id="fund-1"><funding-source>Royal Museum for Central Africa Tervuren</funding-source></award-group><award-group id="fund-2"><funding-source>Zoological Museum Copenhagen</funding-source></award-group><award-group id="fund-3"><funding-source>Natural History Museum of Stockholm</funding-source><award-id>BE-TAF-1649</award-id><award-id>DK-TAF-2183</award-id><award-id>SE-TAF-3009</award-id></award-group><funding-statement>FG acknowledges Synthesys travel grants to visit the Royal Museum for Central Africa Tervuren, the Zoological Museum Copenhagen, and the Natural History Museum of Stockholm (BE-TAF-1649, DK-TAF-2183, DE-TAF-2114, SE-TAF-3009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group></article-meta></front><body><sec><title>Introduction</title><p>The number of cervical vertebrae in mammals is remarkably constant at seven. In other tetrapods, the number of cervical vertebrae varies considerably, and in mammals the number of vertebrae in more caudal vertebral regions is variable as well (<xref rid="ref-15" ref-type="bibr">Leboucq, 1898</xref>; <xref rid="ref-25" ref-type="bibr">Schultz, 1961</xref>; <xref rid="ref-27" ref-type="bibr">Starck, 1979</xref>; <xref rid="ref-20" ref-type="bibr">Narita & Kuratani, 2005</xref>). Only manatees (<italic>Trichechus</italic>, Sirenia) and sloths (<italic>Bradypus</italic> and <italic>Choloepus</italic>, Xenarthra) have an exceptional number of cervical vertebrae (<xref rid="ref-2" ref-type="bibr">Bateson, 1894</xref>; <xref rid="ref-27" ref-type="bibr">Starck, 1979</xref>; <xref rid="ref-30" ref-type="bibr">Varela-Lasheras et al., 2011</xref>). Despite the extreme evolutionary conservation of the number of cervical vertebrae, intraspecific variation is not uncommon in mammals. The most common variation is represented by ribs on the seventh vertebra, so-called cervical ribs, which can be considered a partial or complete homeotic transformation of a cervical into a thoracic vertebra (involving a change in the activity of <italic>Hox</italic> genes (<xref rid="ref-10" ref-type="bibr">Galis, 1999</xref>; <xref rid="ref-17" ref-type="bibr">Li & Shiota, 2000</xref>; <xref rid="ref-30" ref-type="bibr">Varela-Lasheras et al., 2011</xref>; <xref rid="ref-31" ref-type="bibr">Wéry et al., 2003</xref>)). The strong conservation of the number of cervical vertebrae implies that there must be selection against intraspecific variation of this number. Indeed, very strong selection against cervical ribs was shown to exist in humans (<xref rid="ref-10" ref-type="bibr">Galis, 1999</xref>; <xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>; <xref rid="ref-9" ref-type="bibr">Furtado et al., 2011</xref>; <xref rid="ref-29" ref-type="bibr">ten Broek et al., 2012</xref>). Approximately 90 percent of individuals possessing a cervical rib die before reaching reproductive age (<xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>). The severe selection is due to the strong association of cervical ribs with multiple and major congenital abnormalities. In other mammalian species, we have also found an association with abnormalities (<xref rid="ref-30" ref-type="bibr">Varela-Lasheras et al., 2011</xref>). A cervical rib itself is relatively harmless, but its development is induced by a (genetic or environmental) disturbance of early embryogenesis (<xref rid="ref-17" ref-type="bibr">Li & Shiota, 2000</xref>; <xref rid="ref-31" ref-type="bibr">Wéry et al., 2003</xref>; <xref rid="ref-6" ref-type="bibr">Chernoff & Rogers, 2004</xref>; <xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>). Such a disturbance usually has multiple effects, due to the highly interactive nature of early embryogenesis. Hence, the strong selection against cervical ribs is indirect and due to the severity of the associated medical problems (<xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>; <xref rid="ref-29" ref-type="bibr">ten Broek et al., 2012</xref>).</p><p>Of three caudal cervical vertebrae from <italic>Mammuthus primigenius</italic>, a sixth (C6) and two seventh (C7), that were recently found in the North Sea, during infrastructural works for an extension of the Rotterdam Harbour (Maasvlakte 2) and donated to the Natural History Museum in Rotterdam, two possessed articulation facets for cervical ribs (the C6 and one of the C7). This surprising finding aroused our interest, and we searched the extensive collection of Late Pleistocene <italic>M. primigenius</italic> material in the Naturalis Biodiversity Centre (Leiden) to make an estimate of the incidence of this developmental abnormality. Additionally, we determined for comparison the incidence of cervical ribs in skeletons of the most closely related extant species, the Asian and African elephants (<italic>Elephas maximus</italic> and <italic>Loxodonta africana</italic>).</p></sec><sec sec-type="methods"><title>Methods</title><sec><title>Specimens</title><p>We analyzed 6 sixth cervical vertebrae (C6) and 10 seventh cervical vertebrae (C7) of Late Pleistocene mammoths (<italic>M. primigenius</italic>), from two collections: the Natural History Museum Rotterdam (NMR, <xref ref-type="table" rid="table-1">Table 1</xref>) and Naturalis Biodiversity Center (Naturalis, <xref ref-type="table" rid="table-1">Table 1</xref>). The cervical vertebrae were identified as C6 and C7 based on the relative size of the spinous processes and anterior tubercles. We analysed 28 specimens of extant elephants, 21 <italic>E. maximus</italic> and 7 <italic>L. africana</italic>, from 5 collections: the Natural History Museum of Denmark, Copenhagen (ZMUC), Naturhistorisches Museum Wien, Vienna (NHMW), The University of Vienna, the Swedish Museum of Natural History, Stockholm (NRM), the Royal Museum for Central Africa Tervuren (RMCA) and Naturalis Biodiversity Center (Naturalis). All mammoth specimens (see <xref ref-type="table" rid="table-1">Table 1</xref> for collection numbers) are of Late Pleistocene age and originate from the North Sea. Two specimens (C6, inv.nr. NMR999100006627 and C7, inv. nr. NMR999100007602) were recently found during infrastructural works in the Rotterdam harbor area (“Maasvlakte 2”) on the North Sea seabed (Maasvlakte Zandwingebied, i.e., the source area for sand extraction, c. 51°59′N/3°53′E) and allocated to the NMR by the Rotterdam Port Authorities.</p><table-wrap id="table-1" orientation="portrait" position="float"><object-id pub-id-type="doi">10.7717/peerj.318/table-1</object-id><label>Table 1</label><caption><title>List of investigated specimens and scores of articulation facets of cervical ribs.</title><p>The presence of articulation facets of ribs was indicated posteriorly on the sixth cervical vertebra (C6) and/or anteriorly on the seventh cervical vertebra (C7).</p></caption><alternatives><graphic xlink:href="peerj-02-318-g002"></graphic><table frame="hsides" rules="groups"><colgroup span="1"><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col><col span="1"></col></colgroup><thead><tr><th rowspan="1" colspan="1">Species</th><th rowspan="1" colspan="1">Institute</th><th rowspan="1" colspan="1">Collection no.</th><th rowspan="1" colspan="1">Sex</th><th rowspan="1" colspan="1">Vertebra</th><th rowspan="1" colspan="1">Rib facets (left/right)</th></tr></thead><tbody><tr><td rowspan="16" colspan="1"><italic>Mammuthus primigenius</italic></td><td rowspan="13" colspan="1">Naturalis</td><td rowspan="1" colspan="1">RGM592809</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RGM103337</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM132902</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RGM139079</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RGM172327</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM20026</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM20313</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM369465</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM40098</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RGM40120</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RGM4445989</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM79245</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">n.a.</td></tr><tr><td rowspan="1" colspan="1">RGM146248</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">1 (left)</td></tr><tr><td rowspan="3" colspan="1">NMR</td><td rowspan="1" colspan="1">NMR999100007602</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">1 (left)</td></tr><tr><td rowspan="1" colspan="1">NMR999100006627</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6</td><td rowspan="1" colspan="1">1 (right)</td></tr><tr><td rowspan="1" colspan="1">NMR999100007479</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="21" colspan="1"><italic>Elephas maximus</italic></td><td rowspan="7" colspan="1">Naturalis</td><td rowspan="1" colspan="1">RMNH.MAM.46016</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RMNH.MAM.46024</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RMNH.MAM.39235</td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RMNH.MAM.39234</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMA 13483</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RMNH.MAM.46018</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMA.MAM.30069</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="4" colspan="1">NRM</td><td rowspan="1" colspan="1">A609596<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">A591540</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">A600572</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">A589489<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="2" colspan="1">NMW</td><td rowspan="1" colspan="1">16545</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">5505<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">UAV</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="7" colspan="1">ZMUC</td><td rowspan="1" colspan="1">ZMUC CN2</td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN4196<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN1399<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN1</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN2293<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN639<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">F</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">1 (right, C7)</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN 558<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="7" colspan="1"><italic>Loxodonta africana</italic></td><td rowspan="1" colspan="1">Naturalis</td><td rowspan="1" colspan="1">RMNH.MAM.45488</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="2" colspan="1">NRM</td><td rowspan="1" colspan="1">A601286</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">A600551</td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">NMW</td><td rowspan="1" colspan="1">287<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref> (exhibition)</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">RMCA</td><td rowspan="1" colspan="1">RMCA 4559</td><td rowspan="1" colspan="1">n.a.</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="2" colspan="1">ZMUC</td><td rowspan="1" colspan="1">ZMUC CN708<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr><tr><td rowspan="1" colspan="1">ZMUC CN3684<xref ref-type="fn" rid="table-1fn1"><sup>*</sup></xref></td><td rowspan="1" colspan="1">M</td><td rowspan="1" colspan="1">C6, C7</td><td rowspan="1" colspan="1">0</td></tr></tbody></table></alternatives><table-wrap-foot><fn id="table-1fn"><p><bold>Notes.</bold></p></fn><fn id="table-1fn1"><label>*</label><p>Died in captivity (wild born).</p></fn><fn id="table-1fn2" fn-type="other"><p><def-list id="dl1"><def-item><term>n.a.</term><def><p>not available</p></def></def-item><def-item><term>Naturalis</term><def><p>Naturalis Biodiversity Center Leiden</p></def></def-item><def-item><term>NRM</term><def><p>Naturhistoriska Riksmuseet Stockholm</p></def></def-item><def-item><term>NMW</term><def><p>Naturhistorisches Museum Wien</p></def></def-item><def-item><term>UAV</term><def><p>University Anatomy Vienna</p></def></def-item><def-item><term>ZMUC</term><def><p>Zoologisk Museum University Copenhagen</p></def></def-item><def-item><term>RMCA</term><def><p>Royal Museum Central Africa Tervuren</p></def></def-item></def-list></p></fn></table-wrap-foot></table-wrap></sec><sec><title>Cervical ribs</title><p>We analyzed the C6 and C7 vertebrae for the presence or absence of articulation facets of cervical ribs. The presence of cervical ribs can be deduced from articulation facets on the anterior side of C7 (<xref ref-type="fig" rid="fig-1">Figs. 1A</xref> and <xref ref-type="fig" rid="fig-1">1D</xref>) and, if the cervical ribs are large enough, on the posterior side of C6, as well (<xref ref-type="fig" rid="fig-1">Figs. 1B</xref> and <xref ref-type="fig" rid="fig-1">1C</xref>).</p><fig id="fig-1" orientation="portrait" position="float"><object-id pub-id-type="doi">10.7717/peerj.318/fig-1</object-id><label>Figure 1</label><caption><title>Presence of rib articulation facets on cervical vertebrae of woolly mammoths (A–C) and Asian elephant (D).</title><p>(A) Posterior view of a C6 of a <italic>Mammuthus primigenius</italic> from the North Sea (NMR999100006627), showing an articulation facet of a cervical rib on the right side. (B) Anterior view of a C7 of a <italic>Mammuthus primigenius</italic> from the North Sea (NMR999100007602), showing a sinistral articulation facet (lower right in the picture). (C) Posterior view of a C6 of a <italic>Mammuthus primigenius</italic> from the North Sea (Naturalis St 146248), showing an articulation facet of a cervical rib on the left side. (D) Anterior view of a C7 of an <italic>Elephas maximus</italic> (ZMUC CN639), showing a minute articulation facet of a cervical rib on the right side (see inset for articulation facet). The size of cervical ribs is presumably associated with the strength of associated abnormalities. Arrows indicate articulation facets.</p></caption><graphic xlink:href="peerj-02-318-g001"></graphic></fig></sec><sec><title>Statistical tests</title><p>To compare the prevalence of cervical rib facets between mammoths and elephants we used a G-test of independence, which is particularly appropriate for variable samples sizes as is often the case with paleopathological data (<xref rid="ref-8" ref-type="bibr">Farke, 2007</xref>). Furthermore we also used Barnard’s test for 2 × 2 tables, which is appropriate for small sample sizes and yields greater power than Fisher’s exact test (<xref rid="ref-1" ref-type="bibr">Barnard, 1945</xref>). P-values <0.05 were considered as significant. All analyses were carried out in R.</p></sec></sec><sec sec-type="results"><title>Results</title><p>Articulation facets for cervical ribs on cervical vertebrae are characterized by the following combination of characteristics: (i) they have a smooth, polished-looking surface, visibly smoother than the (surrounding) cortical surface of the vertebrae; (ii) the surfaces have no vascular or nervous foramina; and (iii) the facets are bordered by a clear edge, distinguishing them from the surrounding cortex.</p><p>We found one C7 with a unilateral sinistral anterior rib facet indicating a left cervical rib (<xref ref-type="fig" rid="fig-1">Fig. 1A</xref>). Five C7 did not have rib facets anteriorly and four could not be judged due to the absence of the relevant part of the vertebra. We found two C6 with rib facets on the posterior side indicating cervical ribs: one on the right side and one on the left side (<xref ref-type="fig" rid="fig-1">Figs. 1B</xref> and <xref ref-type="fig" rid="fig-1">1C</xref> respectively). We found one C6 without rib facets posteriorly and three that could not be judged.</p><p>Thus, out of the nine C6 and C7 that could be evaluated, three indicate the presence of a cervical rib, i.e., an incidence of cervical rib facets of 33.3%. We found in one of the 21 <italic>E. maximus</italic> a minute cervical rib facet on C7 (<xref ref-type="fig" rid="fig-1">Fig. 1D</xref>, 4.8%) and no articulation facet visible posteriorly on C6 of the same individual. None of the seven <italic>L. africana</italic> individuals had cervical rib facets, nor were rudimentary cervical ribs found. The overall incidence of cervical ribs in the two species is, thus, 3.6%. This is significantly lower than the 33.3% in mammoths, if we only consider vertebrae that can be evaluated for cervical rib articulation facets (G-test for independence, <italic>p</italic> = 0.035, Barnard’s exact test, <italic>p</italic> = 0.031).</p></sec><sec sec-type="discussion"><title>Discussion</title><p>The incidence of cervical rib facets in our set of Late Pleistocene <italic>M. primigenius</italic> recovered from the North Sea is extremely high (3 out of 9, 33.3%), almost ten times higher than that of extant elephants (1 out of 29, 3.6%). In humans, an incidence higher than 1% has only been found in hospitals or isolated populations (<xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>). An incidence higher than 25% has only been found in children with leukemia, brain tumours and neuroblastoma (<xref rid="ref-26" ref-type="bibr">Schumacher, Mai & Gutjahr, 1992</xref>; <xref rid="ref-11" ref-type="bibr">Galis & Metz, 2003</xref>; <xref rid="ref-18" ref-type="bibr">Merks et al., 2005</xref>) and in deceased fetuses and infants (<xref rid="ref-12" ref-type="bibr">Galis et al., 2006</xref>; <xref rid="ref-9" ref-type="bibr">Furtado et al., 2011</xref>; <xref rid="ref-29" ref-type="bibr">ten Broek et al., 2012</xref>). Along with the high incidence of cervical ribs in mammoths, the size of the articulation facets is particularly large (<xref ref-type="fig" rid="fig-1">Figs. 1A</xref>–<xref ref-type="fig" rid="fig-1">1C</xref>), substantially larger than the articulation facet found in the one <italic>E. maximus</italic> (<xref ref-type="fig" rid="fig-1">Fig. 1D</xref>) and, pointing to substantially larger cervical ribs than usually found in humans (see <xref rid="ref-3" ref-type="bibr">Bots et al., 2011</xref>; <xref rid="ref-29" ref-type="bibr">ten Broek et al., 2012</xref> for examples). Size of cervical ribs was found to be negatively correlated with fitness in transgenic mice (<xref rid="ref-13" ref-type="bibr">Jeannotte et al., 1993</xref>; see also <xref rid="ref-3" ref-type="bibr">Bots et al., 2011</xref>).</p><p>The exceptionally high incidence of large cervical ribs in our set of Late Pleistocene <italic>mammoths</italic> can be due to two factors. Firstly, it can be due to a high rate of inbreeding in declining populations, before final extinction. A high incidence of cervical ribs (7.46%) has been observed in an isolated human population (<xref rid="ref-22" ref-type="bibr">Palma & Carini, 1990</xref>) in Sicily, in inbred pedigreed dogs (11.4% <xref rid="ref-5" ref-type="bibr">Breit & Kunzel, 1998</xref>) and inbred minipigs (11% at birth, <xref rid="ref-14" ref-type="bibr">Jørgensen, 1998</xref>). Generally, in inbred mammals there is an increased incidence of congenital anomalies (<xref rid="ref-7" ref-type="bibr">Cristescu et al., 2009</xref>; <xref rid="ref-23" ref-type="bibr">Räikkönen et al., 2013</xref>). Recent studies have shown that the genetic diversity was extremely low in Late Pleistocene mammoth populations in Siberia (<xref rid="ref-19" ref-type="bibr">Miller et al., 2008</xref>; <xref rid="ref-21" ref-type="bibr">Nyström et al., 2012</xref>). Additionally, the increased incidence of cervical ribs may be due to harsh conditions that impact early pregnancies, because diseases, famine, cold and other stressors can lead to disturbances of early organogenesis, that can result in the induction of cervical ribs (e.g., <xref rid="ref-24" ref-type="bibr">Sawin, 1937</xref>; <xref rid="ref-17" ref-type="bibr">Li & Shiota, 2000</xref>; <xref rid="ref-31" ref-type="bibr">Wéry et al., 2003</xref>; <xref rid="ref-6" ref-type="bibr">Chernoff & Rogers, 2004</xref>; <xref rid="ref-28" ref-type="bibr">Steigenga et al., 2006</xref>). Harsh conditions during the Late Pleistocene, a period of intense climatic fluctuations and ecosystem instability, are plausible (<xref rid="ref-4" ref-type="bibr">Brace et al., 2012</xref>). Furthermore, bone dystrophy in mammoth calves of Northern Eurasian Late Pleistocene populations is found regularly and assumed to be caused by mineral deficiencies in pregnant females (<xref rid="ref-16" ref-type="bibr">Leshchinskiy, 2012</xref>). Hence, a combination of inbreeding and harsh conditions may be the most likely explanation for the extremely high incidence of cervical ribs. Our results, thus, are in agreement with inbreeding in populations in North-Western Eurasia, just as has been found for Siberian populations (<xref rid="ref-19" ref-type="bibr">Miller et al., 2008</xref>; <xref rid="ref-21" ref-type="bibr">Nyström et al., 2012</xref>). Finally, the high incidence and large size of the cervical ribs indicates a strong vulnerability, given the association of cervical ribs with diseases and congenital abnormalities in mammals. The vulnerable condition may well have contributed to the eventual extinction of the woolly mammoths.</p></sec></body><back><ack><p>We thank the Rotterdam Port Authorities for the donation of all bones that are found during the extension of the Rotterdam harbor in the North Sea to the Natural History Museum in Rotterdam. We thank Mogens Andersen, Alex Bibl, Daniela Kalthoff, Steven van der Mije, Wim Wendelen and Reinier van Zelst for making specimens available and Alexandra van der Geer, Jacques van Alphen, Russell Lande, Natasja den Ouden and Rienk de Jong for comments. We thank Joris van Alphen for making the photographs of <xref ref-type="fig" rid="fig-1">Figs. 1A</xref>–<xref ref-type="fig" rid="fig-1">1C</xref>.</p></ack><sec sec-type="additional-information"><title>Additional Information and Declarations</title><fn-group content-type="competing-interests"><title>Competing Interests</title><fn id="conflict-1" fn-type="con"><p>The authors declare no competing interests.</p></fn></fn-group><fn-group content-type="author-contributions"><title>Author Contributions</title><fn id="contribution-1" fn-type="con"><p><xref ref-type="contrib" rid="author-1">Jelle W.F. Reumer</xref> and <xref ref-type="contrib" rid="author-3">Frietson Galis</xref> conceived and designed the experiments, performed the experiments, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper.</p></fn><fn id="contribution-2" fn-type="con"><p><xref ref-type="contrib" rid="author-2">Clara M.A. ten Broek</xref> performed the experiments, analyzed the data, prepared figures and/or tables, reviewed drafts of the paper.</p></fn></fn-group></sec><ref-list content-type="authoryear"><title>References</title><ref id="ref-1"><label>Barnard (1945)</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Barnard</surname><given-names>G</given-names></name></person-group><article-title>A new test for 2 × 2 tables</article-title><source>Nature</source><year>1945</year><volume>156</volume><fpage>783</fpage><lpage>784</lpage><pub-id pub-id-type="doi">10.1038/156783b0</pub-id></element-citation></ref><ref id="ref-2"><label>Bateson (1894)</label><element-citation publication-type="book"><person-group person-group-type="author"><name><surname>Bateson</surname><given-names>W</given-names></name></person-group><source>Materials for the study of variation</source><year>1894</year><publisher-loc>London</publisher-loc><publisher-name>MacMillan</publisher-name></element-citation></ref><ref id="ref-3"><label>Bots et al. 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