{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T15:14:05Z","timestamp":1791386045582,"version":"4.3.3"},"reference-count":111,"publisher":"The Royal Society","issue":"1663","license":[{"start":{"date-parts":[[2015,3,5]],"date-time":"2015-03-05T00:00:00Z","timestamp":1425513600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Phil. Trans. R. Soc. B"],"published-print":{"date-parts":[[2015,3,5]]},"abstract":"<jats:p>The placenta is one of the most morphologically variable mammalian organs. Four major characteristics are typically discussed when comparing the placentas of different eutherian species: placental shape, maternal\u2013fetal interdigitation, intimacy of the maternal\u2013fetal interface and the pattern of maternal\u2013fetal blood flow. Here, we describe the evolution of three of these features as well as other key aspects of eutherian placentation. In addition to interspecific anatomical variation, there is also variation in placental anatomy and function within a single species. Much of this intraspecific variation occurs in response to different environmental conditions such as altitude and poor maternal nutrition. Examinations of variation in the placenta from both intra- and interspecies perspectives elucidate different aspects of placental function and dysfunction at the maternal\u2013fetal interface. Comparisons within species identify candidate mechanisms that are activated in response to environmental stressors ultimately contributing to the aetiology of obstetric syndromes such as pre-eclampsia. Comparisons above the species level identify the evolutionary lineages on which the potential for the development of obstetric syndromes emerged.<\/jats:p>","DOI":"10.1098\/rstb.2014.0072","type":"journal-article","created":{"date-parts":[[2015,1,19]],"date-time":"2015-01-19T22:59:03Z","timestamp":1421708343000},"page":"20140072","update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":54,"title":["A review of inter- and intraspecific variation in the eutherian placenta"],"prefix":"10.1098","volume":"370","author":[{"suffix":"Jr","given":"William E.","family":"Gundling","sequence":"first","affiliation":[{"name":"Institute for Genomic Biology, University of Illinois, Urbana, IL, USA"},{"name":"Department of Molecular and Integrative Physiology, University of Illinois, Urbana, IL, USA"},{"name":"Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Derek E.","family":"Wildman","sequence":"additional","affiliation":[{"name":"Institute for Genomic Biology, University of Illinois, Urbana, IL, USA"},{"name":"Department of Molecular and Integrative Physiology, University of Illinois, Urbana, IL, USA"},{"name":"Center for Molecular Medicine and Genetics, Wayne State University, Detroit, MI, USA"},{"name":"Department of Obstetrics and Gynecology, Wayne State University, Detroit, MI, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2015,3,5]]},"reference":[{"key":"e_1_3_3_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2011.12.003"},{"key":"e_1_3_3_3_2","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/179827"},{"key":"e_1_3_3_4_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0511344103"},{"key":"e_1_3_3_5_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4757-4199-5"},{"key":"e_1_3_3_6_2","doi-asserted-by":"publisher","DOI":"10.1152\/jappl.1995.79.1.15"},{"key":"e_1_3_3_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-3016.1992.tb00764.x"},{"key":"e_1_3_3_8_2","doi-asserted-by":"publisher","DOI":"10.1079\/PNS19980019"},{"key":"e_1_3_3_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2009.08.004"},{"key":"e_1_3_3_10_2","doi-asserted-by":"publisher","DOI":"10.1002\/jez.b.21079"},{"key":"e_1_3_3_11_2","doi-asserted-by":"publisher","DOI":"10.1071\/RD08009"},{"key":"e_1_3_3_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2012.11.021"},{"key":"e_1_3_3_13_2","doi-asserted-by":"publisher","DOI":"10.1186\/1477-7827-2-46"},{"key":"e_1_3_3_14_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-540-78797-6"},{"key":"e_1_3_3_15_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2012.07.004"},{"key":"e_1_3_3_16_2","first-page":"5","article-title":"The guinea-pig placenta","volume":"53","author":"Kaufmann P","year":"1977","journal-title":"Adv. Anat. Embryol. Cell Biol."},{"key":"e_1_3_3_17_2","doi-asserted-by":"publisher","DOI":"10.1002\/aja.1001590208"},{"key":"e_1_3_3_18_2","doi-asserted-by":"publisher","DOI":"10.1186\/1477-7827-10-102"},{"key":"e_1_3_3_19_2","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/978-1-4614-4060-4_3","volume-title":"Building babies. developments in primatology: progress and prospects","author":"Sterner K","year":"2013"},{"key":"e_1_3_3_20_2","first-page":"142","article-title":"Comparative development and evolution of the placenta in primates","volume":"3","author":"Luckett WP","year":"1974","journal-title":"Contrib. Primatol."},{"key":"e_1_3_3_21_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpa.2007.01.029"},{"key":"e_1_3_3_22_2","unstructured":"Benirschke K. 2007 Comparative Placentation 2007 (updated 1\/19\/2012; cited 2007). See http:\/\/placentation.ucsd.edu\/index.html."},{"key":"e_1_3_3_23_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-349-09065-5"},{"key":"e_1_3_3_24_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0704342104"},{"key":"e_1_3_3_25_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1211028"},{"key":"e_1_3_3_26_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature05634"},{"key":"e_1_3_3_27_2","first-page":"378","article-title":"Formation of syncytium from cytotrophoblast in the human placenta","volume":"25","author":"Enders AC","year":"1965","journal-title":"Obstet. Gynecol."},{"key":"e_1_3_3_28_2","doi-asserted-by":"publisher","DOI":"10.1038\/nri1897"},{"key":"e_1_3_3_29_2","doi-asserted-by":"publisher","DOI":"10.1530\/REP-10-0360"},{"key":"e_1_3_3_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.yhbeh.2010.06.007"},{"key":"e_1_3_3_31_2","doi-asserted-by":"publisher","DOI":"10.1097\/PSY.0b013e318177940d"},{"key":"e_1_3_3_32_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1308998110"},{"key":"e_1_3_3_33_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.138487.112"},{"key":"e_1_3_3_34_2","first-page":"639","article-title":"Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects","volume":"17","author":"Ben-Jonathan N","year":"1996","journal-title":"Endocr. Rev."},{"key":"e_1_3_3_35_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msr189"},{"key":"e_1_3_3_36_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.cellbio.24.110707.175418"},{"key":"e_1_3_3_37_2","first-page":"342","article-title":"Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis","volume":"15","author":"Simpson ER","year":"1994","journal-title":"Endocr. Rev."},{"key":"e_1_3_3_38_2","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.20756"},{"key":"e_1_3_3_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-0760(01)00156-X"},{"key":"e_1_3_3_40_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1432-1327.1999.00734.x"},{"key":"e_1_3_3_41_2","doi-asserted-by":"publisher","DOI":"10.1210\/jcem-65-4-757"},{"key":"e_1_3_3_42_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0707873105"},{"key":"e_1_3_3_43_2","doi-asserted-by":"publisher","DOI":"10.1053\/plac.2001.0722"},{"key":"e_1_3_3_44_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0406509102"},{"key":"e_1_3_3_45_2","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms4966"},{"key":"e_1_3_3_46_2","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.105.039941"},{"key":"e_1_3_3_47_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cellsig.2013.11.002"},{"key":"e_1_3_3_48_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M209316200"},{"key":"e_1_3_3_49_2","doi-asserted-by":"publisher","DOI":"10.1210\/mend.13.3.0243"},{"key":"e_1_3_3_50_2","first-page":"1579","article-title":"Coordinate control of the alpha- and beta-subunit genes of human chorionic gonadotropin by trophoblast-specific element-binding protein","volume":"7","author":"Steger DJ","year":"1993","journal-title":"Mol. Endocrinol."},{"key":"e_1_3_3_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.mehy.2011.02.017"},{"key":"e_1_3_3_52_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkt1196"},{"key":"e_1_3_3_53_2","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.20673"},{"key":"e_1_3_3_54_2","doi-asserted-by":"publisher","DOI":"10.1006\/geno.2000.6302"},{"key":"e_1_3_3_55_2","doi-asserted-by":"publisher","DOI":"10.1002\/mrd.20272"},{"key":"e_1_3_3_56_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tem.2011.09.003"},{"key":"e_1_3_3_57_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0903568106"},{"key":"e_1_3_3_58_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2014.07.015"},{"key":"e_1_3_3_59_2","doi-asserted-by":"publisher","DOI":"10.1210\/en.2014-1501"},{"key":"e_1_3_3_60_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0897.2010.00929.x"},{"key":"e_1_3_3_61_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2006.11.002"},{"key":"e_1_3_3_62_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0013663"},{"key":"e_1_3_3_63_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0897.2008.00580.x"},{"key":"e_1_3_3_64_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1600-0897.1999.tb00071.x"},{"key":"e_1_3_3_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jri.2014.02.006"},{"key":"e_1_3_3_66_2","doi-asserted-by":"publisher","DOI":"10.1038\/35080570"},{"key":"e_1_3_3_67_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1440-1681.2008.04975.x"},{"key":"e_1_3_3_68_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00318873"},{"key":"e_1_3_3_69_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0143-4004(05)80255-3"},{"key":"e_1_3_3_70_2","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1973.sp010393"},{"key":"e_1_3_3_71_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jri.2013.06.002"},{"key":"e_1_3_3_72_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1471-0528.1986.tb07830.x"},{"key":"e_1_3_3_73_2","doi-asserted-by":"publisher","DOI":"10.1161\/01.HYP.0000188408.49896.c5"},{"key":"e_1_3_3_74_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1111726"},{"key":"e_1_3_3_75_2","doi-asserted-by":"publisher","DOI":"10.1161\/HYPERTENSIONAHA.113.01892"},{"key":"e_1_3_3_76_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-pathol-011110-130315"},{"key":"e_1_3_3_77_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2011.10.003"},{"key":"e_1_3_3_78_2","doi-asserted-by":"publisher","DOI":"10.1034\/j.1600-0897.2002.1o043.x"},{"key":"e_1_3_3_79_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bpobgyn.2010.10.010"},{"key":"e_1_3_3_80_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2011.05.007"},{"key":"e_1_3_3_81_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2011.02.009"},{"key":"e_1_3_3_82_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2012.12.001"},{"key":"e_1_3_3_83_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.placenta.2004.01.008"},{"key":"e_1_3_3_84_2","doi-asserted-by":"publisher","DOI":"10.1089\/152702903322022785"},{"key":"e_1_3_3_85_2","doi-asserted-by":"publisher","DOI":"10.1007\/0-306-46825-5_6"},{"key":"e_1_3_3_86_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0701985104"},{"key":"e_1_3_3_87_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.resp.2007.05.013"},{"key":"e_1_3_3_88_2","doi-asserted-by":"publisher","DOI":"10.1089\/15270290152608598"},{"key":"e_1_3_3_89_2","doi-asserted-by":"publisher","DOI":"10.1038\/hdy.2011.85"},{"key":"e_1_3_3_90_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1001116"},{"key":"e_1_3_3_91_2","doi-asserted-by":"publisher","DOI":"10.1093\/emboj\/cdg392"},{"key":"e_1_3_3_92_2","doi-asserted-by":"publisher","DOI":"10.1002\/ajhb.21167"},{"key":"e_1_3_3_93_2","first-page":"70","article-title":"The Dutch famine, 1944\u20131945, and the reproductive process. I. Effects on six indices at birth","volume":"9","author":"Stein Z","year":"1975","journal-title":"Pediatr. Res."},{"key":"e_1_3_3_94_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1001252"},{"key":"e_1_3_3_95_2","doi-asserted-by":"publisher","DOI":"10.4161\/epi.6.2.13516"},{"key":"e_1_3_3_96_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0806560105"},{"key":"e_1_3_3_97_2","doi-asserted-by":"publisher","DOI":"10.1159\/000090843"},{"key":"e_1_3_3_98_2","doi-asserted-by":"publisher","DOI":"10.1042\/cs0950115"},{"key":"e_1_3_3_99_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1523-1755.1999.00633.x"},{"key":"e_1_3_3_100_2","doi-asserted-by":"publisher","DOI":"10.1017\/S2040174409990171"},{"key":"e_1_3_3_101_2","first-page":"648","article-title":"Mother\u2013offspring conflict","volume":"12","author":"Trivers RL","year":"1972","journal-title":"Am. Zool."},{"key":"e_1_3_3_102_2","doi-asserted-by":"publisher","DOI":"10.1093\/icb\/14.1.249"},{"key":"e_1_3_3_103_2","first-page":"113","article-title":"Genomic imprinting and the evolution of human childhood","volume":"14","author":"Haig D","year":"2002","journal-title":"Am. J. Hum. Biol."},{"key":"e_1_3_3_104_2","doi-asserted-by":"publisher","DOI":"10.1016\/0168-9525(91)90230-N"},{"key":"e_1_3_3_105_2","doi-asserted-by":"publisher","DOI":"10.1080\/10641950701826711"},{"key":"e_1_3_3_106_2","doi-asserted-by":"publisher","DOI":"10.1086\/418300"},{"key":"e_1_3_3_107_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.genom.122007.110031"},{"key":"e_1_3_3_108_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.mam.2012.06.009"},{"key":"e_1_3_3_109_2","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1997.0230"},{"key":"e_1_3_3_110_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.psyneuen.2012.05.014"},{"key":"e_1_3_3_111_2","first-page":"320","article-title":"Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates","volume":"7","author":"Medawar PB","year":"1953","journal-title":"Symp. Soc. Exp. Biol."},{"key":"e_1_3_3_112_2","doi-asserted-by":"publisher","DOI":"10.1080\/14767050902784171"}],"container-title":["Philosophical Transactions of the Royal Society B: Biological Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rstb.2014.0072","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rstb.2014.0072","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rstb.2014.0072","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T21:27:36Z","timestamp":1778621256000},"score":1,"resource":{"primary":{"URL":"http:\/\/royalsocietypublishing.org\/rstb\/article\/22411"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,3,5]]},"references-count":111,"journal-issue":{"issue":"1663","published-print":{"date-parts":[[2015,3,5]]}},"alternative-id":["10.1098\/rstb.2014.0072"],"URL":"https:\/\/doi.org\/10.1098\/rstb.2014.0072","relation":{},"ISSN":["0962-8436","1471-2970"],"issn-type":[{"value":"0962-8436","type":"print"},{"value":"1471-2970","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,3,5]]},"assertion":[{"value":"2015-03-05","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}