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The structural diversity of the mammalian placenta is remarkable, despite sharing a single common ancestor and conserved physiological functions. Historically, investigations into the evolution of the mammalian placenta have been grounded in \u2018the efficiency paradigm\u2019, i.e. the assumption that certain placental configurations permit easier nutrient exchange, but this paradigm has struggled to explain the diversity of mammalian placentation strategies. Here, we propose a new paradigm to understand mammalian placental evolution. Using multidimensional plotting of recorded placental structures, quantitative metrics for mammalian maternal investment, and illustrative computational modelling of physiological processes, we argue that the ancestral mammalian placenta is not a streamlined \u2018highly efficient\u2019 design, but rather a product of low maternal investment, with fitness costs that manifest as gestational demand increases. Expansion of small mammals into larger\u2010bodied, longer\u2010lived niches induces a \u2018placental crisis\u2019 characterised by maternal under\u2010investment and chronic gestational dysfunction, triggering an arms race through the interaction of disruptive selection and materno\u2010fetal conflict. We propose the acute severity of the placental crisis is the foundation of placental evolution. We go on to argue that some primates are currently in a state of placental crisis and that maternal under\u2010investment and inappropriate placentation are the evolutionary foundations of human gestational dysfunctions such as pre\u2010eclampsia. We conclude that the ancestral mammalian placenta was not an efficiently optimised design that allowed placentation to dominate the clade, but rather an idiosyncrasy of mammal\u2010specific biology, which likely hindered mammalian expansion into larger\u2010bodied niches.<\/jats:p>","DOI":"10.1002\/brv.70139","type":"journal-article","created":{"date-parts":[[2026,1,31]],"date-time":"2026-01-31T08:26:47Z","timestamp":1769848007000},"page":"1627-1640","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Placental crises: disruptive selection and maternal under\u2010investment as the foundations of mammalian placental evolution and dysfunction"],"prefix":"10.1002","volume":"101","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1508-664X","authenticated-orcid":false,"given":"Davis","family":"Laundon","sequence":"first","affiliation":[{"name":"School of Human Development and Health, Faculty of Medicine, IDS Building University of Southampton, Southampton General Hospital  Southampton SO16 6YD UK"},{"name":"Institute for Life Sciences, University of Southampton  University Rd, Highfield Southampton SO17 1BJ UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5960-7769","authenticated-orcid":false,"given":"Neil J.","family":"Gostling","sequence":"additional","affiliation":[{"name":"Institute for Life Sciences, University of Southampton  University Rd, Highfield Southampton SO17 1BJ UK"},{"name":"School of Biological Sciences, Faculty of Environmental and Life Sciences University of Southampton  University Rd, Highfield Southampton SO17 1BJ UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ian G.","family":"Reddin","sequence":"additional","affiliation":[{"name":"School of Cancer Sciences, Faculty of Medicine, IDS Building University of Southampton  Southampton SO16 6YD UK"},{"name":"Bio\u2010R Bioinformatics Research Facility, Faculty of Medicine, IDS Building University of Southampton  Southampton SO16 6YD UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bram G.","family":"Sengers","sequence":"additional","affiliation":[{"name":"Institute for Life Sciences, University of Southampton  University Rd, Highfield Southampton SO17 1BJ UK"},{"name":"School of Engineering, Faculty of Engineering and Physical Sciences University of Southampton  University Road Southampton SO17 1BJ UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4581-6092","authenticated-orcid":false,"given":"Pascale","family":"Chavatte\u2010Palmer","sequence":"additional","affiliation":[{"name":"Universit\u00e9 Paris\u2010Saclay, UVSQ, INRAE, BREED  Jouy\u2010en\u2010Josas 78350 France"},{"name":"Ecole Nationale V\u00e9t\u00e9rinaire d\u2019Alfort, BREED  Maisons\u2010Alfort 94700 France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rohan M.","family":"Lewis","sequence":"additional","affiliation":[{"name":"School of Human Development and Health, Faculty of Medicine, IDS Building University of Southampton, Southampton General Hospital  Southampton SO16 6YD UK"},{"name":"Institute for Life Sciences, University of Southampton  University Rd, Highfield Southampton SO17 1BJ UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,1,31]]},"reference":[{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.30994"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.1006\/anbe.2001.1786"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1530\/rep.0.1230445"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1080\/106351599260472"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-04341-1"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1959.tb44596.x"},{"key":"e_1_2_9_9_1","first-page":"121","article-title":"Reproductive modes and strategies in vertebrate evolution","volume":"51","author":"Angelini F. 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