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<title xml:lang="en">Diversification of the eutherian placenta is associated with changes in the pace of life</title>
<author>
<name sortKey="Garratt, Michael" sort="Garratt, Michael" uniqKey="Garratt M" first="Michael" last="Garratt">Michael Garratt</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff1">Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences,
<institution>University of New South Wales</institution>
, Sydney, NSW 2052,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gaillard, Jean Michel" sort="Gaillard, Jean Michel" uniqKey="Gaillard J" first="Jean-Michel" last="Gaillard">Jean-Michel Gaillard</name>
<affiliation>
<nlm:aff id="aff2">Université de Lyon, F-69000, Lyon ; Université Lyon 1 ; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne,
<country>France</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brooks, Robert C" sort="Brooks, Robert C" uniqKey="Brooks R" first="Robert C." last="Brooks">Robert C. Brooks</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff1">Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences,
<institution>University of New South Wales</institution>
, Sydney, NSW 2052,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Lemaitre, Jean Francois" sort="Lemaitre, Jean Francois" uniqKey="Lemaitre J" first="Jean-François" last="Lemaître">Jean-François Lemaître</name>
<affiliation>
<nlm:aff id="aff2">Université de Lyon, F-69000, Lyon ; Université Lyon 1 ; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne,
<country>France</country>
</nlm:aff>
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<date when="2013">2013</date>
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<title xml:lang="en" level="a" type="main">Diversification of the eutherian placenta is associated with changes in the pace of life</title>
<author>
<name sortKey="Garratt, Michael" sort="Garratt, Michael" uniqKey="Garratt M" first="Michael" last="Garratt">Michael Garratt</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff1">Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences,
<institution>University of New South Wales</institution>
, Sydney, NSW 2052,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Gaillard, Jean Michel" sort="Gaillard, Jean Michel" uniqKey="Gaillard J" first="Jean-Michel" last="Gaillard">Jean-Michel Gaillard</name>
<affiliation>
<nlm:aff id="aff2">Université de Lyon, F-69000, Lyon ; Université Lyon 1 ; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne,
<country>France</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Brooks, Robert C" sort="Brooks, Robert C" uniqKey="Brooks R" first="Robert C." last="Brooks">Robert C. Brooks</name>
<affiliation>
<nlm:aff wicri:cut=" and" id="aff1">Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences,
<institution>University of New South Wales</institution>
, Sydney, NSW 2052,
<country>Australia</country>
</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Lemaitre, Jean Francois" sort="Lemaitre, Jean Francois" uniqKey="Lemaitre J" first="Jean-François" last="Lemaître">Jean-François Lemaître</name>
<affiliation>
<nlm:aff id="aff2">Université de Lyon, F-69000, Lyon ; Université Lyon 1 ; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne,
<country>France</country>
</nlm:aff>
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<title level="j">Proceedings of the National Academy of Sciences of the United States of America</title>
<idno type="ISSN">0027-8424</idno>
<idno type="eISSN">1091-6490</idno>
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<date when="2013">2013</date>
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<div type="abstract" xml:lang="en">
<p>Few mammalian organs vary as dramatically among species as the placenta. This variation is remarkable considering that the placenta’s primary function—transfer of nutrients and waste between mother and offspring—does not differ among species. Evolutionary changes in placental morphology remain poorly understood, with suggestions that parent–offspring conflict or evolutionary changes in life history might drive placental evolution. Here we demonstrate that life history differences among eutherian mammals are associated with major transitions in maternofetal interdigitation and placental invasiveness. We show that the repeated evolution of villous interdigitation is associated with reduced offspring production early in life and an increased lifespan. Further changes in placental morphology that reestablish a larger surface area are also associated with a change back to greater offspring production. After controlling for these differences in interdigitation, we also show that the least invasive placental type is associated with a fast pace of life. We predict that selection for a faster pace of life intensifies parent–offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the fetus and alter their relative allocation to offspring production across life.</p>
</div>
</front>
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<journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
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<journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
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<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
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<publisher-name>National Academy of Sciences</publisher-name>
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<article-id pub-id-type="doi">10.1073/pnas.1305018110</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Biological Sciences</subject>
<subj-group>
<subject>Evolution</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Diversification of the eutherian placenta is associated with changes in the pace of life</article-title>
<alt-title alt-title-type="short">Placentation and life history</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Garratt</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gaillard</surname>
<given-names>Jean-Michel</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Brooks</surname>
<given-names>Robert C.</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lemaître</surname>
<given-names>Jean-François</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<aff id="aff1">
<sup>a</sup>
Evolution and Ecology Research Centre and School of Biological, Earth, and Environmental Sciences,
<institution>University of New South Wales</institution>
, Sydney, NSW 2052,
<country>Australia</country>
and</aff>
<aff id="aff2">
<sup>b</sup>
Université de Lyon, F-69000, Lyon ; Université Lyon 1 ; CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive, F-69622 Villeurbanne,
<country>France</country>
</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>1</sup>
To whom correspondence should be addressed. E-mail:
<email>Michael.Garratt@unsw.edu.au</email>
.</corresp>
<fn fn-type="edited-by">
<p>Edited by Suzette D. Tardif, University of Texas Health Science Center at San Antonio, San Antonio, TX and accepted by the Editorial Board March 26, 2013 (received for review March 18, 2013)</p>
</fn>
<fn fn-type="con">
<p>Author contributions: M.G. and J.-F.L. designed research; M.G., J.-M.G., and J.-F.L. performed research; M.G., J.-M.G., and J.-F.L. analyzed data; and M.G. and R.C.B. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub">
<day>7</day>
<month>5</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub">
<day>22</day>
<month>4</month>
<year>2013</year>
</pub-date>
<volume>110</volume>
<issue>19</issue>
<fpage>7760</fpage>
<lpage>7765</lpage>
<self-uri xlink:title="pdf" xlink:type="simple" xlink:href="pnas.201305018.pdf"></self-uri>
<abstract>
<p>Few mammalian organs vary as dramatically among species as the placenta. This variation is remarkable considering that the placenta’s primary function—transfer of nutrients and waste between mother and offspring—does not differ among species. Evolutionary changes in placental morphology remain poorly understood, with suggestions that parent–offspring conflict or evolutionary changes in life history might drive placental evolution. Here we demonstrate that life history differences among eutherian mammals are associated with major transitions in maternofetal interdigitation and placental invasiveness. We show that the repeated evolution of villous interdigitation is associated with reduced offspring production early in life and an increased lifespan. Further changes in placental morphology that reestablish a larger surface area are also associated with a change back to greater offspring production. After controlling for these differences in interdigitation, we also show that the least invasive placental type is associated with a fast pace of life. We predict that selection for a faster pace of life intensifies parent–offspring conflict, and that the repeated evolution of less-invasive placental structures might have allowed mothers to wrest back control of gestation from the fetus and alter their relative allocation to offspring production across life.</p>
</abstract>
<kwd-group>
<kwd>aging</kwd>
<kwd>senescence</kwd>
<kwd>reproduction</kwd>
<kwd>placentation</kwd>
</kwd-group>
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<page-count count="6"></page-count>
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</front>
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