The evolutionary significance of placental interdigitation in mammalian reproduction: Contributions from comparative studies
Open accessAbstract
The placenta is fundamental to mammalian reproduction and is surprisingly diverse in gross morphology among species. Whether and how this diversity affects maternal investment and fetal growth is still poorly understood. Contrary to suggestions that highly invasive hemochorial placentation is beneficial to fetal development, recent comparative studies have revealed that interdigitation - the degree of contact between maternal and fetal tissues at the area of exchange - strongly influences fetal growth rates. Species with labyrinthine placentae give birth to neonates of similar size to those of species with villous or trabecular placentae but in less than half the time. These findings suggest that there might be tradeoffs between fetal growth rates (higher with greater interdigitation) and gestation time (shorter with greater interdigitation), in association with type of interdigitation. Such tradeoffs might be the results of maternal-offspring conflict over the allocation of maternal resources, with paternal genes favouring greater interdigitation and so higher fetal growth, and maternal genes responding by reducing gestation time. These results emphasize the role of interdigitation as a means to increase the surface area for exchange, and are consistent with within species studies demonstrating that a higher surface area for exchange is associated with heavier neonates. Further studies could investigate the role of other traits in the evolution of placental diversity and their impact on fetal development.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Species with a labyrinthine placenta have gestation lengths less than half those associated with a villous or folded placenta, although there are no relationships with birth weight or brain size.
“Comparative studies have demonstrated that species with a labyrinthine placenta have gestation lengths less than half those associated with a villous or folded placenta, although there are no relationships with birth weight or brain size (91,92).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [91]
Cites
Inferring the historical patterns of biological evolution
Pagel, M. (1999) · Nature · doi:10.1038/44766 · Cited by 5,200 · see citing works
Trivers, R. L. (1974) · American Zoologist · doi:10.1093/icb/14.1.249 · Cited by 4,210 · see citing works
Phylogenetic Analysis and Comparative Data: A Test and Review of Evidence
Freckleton, R. P., Harvey, P. H., & Pagel, M. (2002) · The American Naturalist · doi:10.1086/343873 · Cited by 2,604 · see citing works
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Genetic conflicts in human pregnancy
Haig, D. (1993) · The Quarterly Review of Biology · doi:10.1086/418300 · Cited by 1,253 · see citing works
Inferring evolutionary processes from phylogenies
PAGEL, M. (1997) · Zoologica Scripta · doi:10.1111/j.1463-6409.1997.tb00423.x · Cited by 1,106 · see citing works
Pathology of the Human Placenta
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · doi:10.1007/978-3-642-23941-0 · Cited by 502 · see citing works
Placental structure: in a comparative aspect
Leiser, R., & Kaufmann, P. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211275 · Cited by 452 · see citing works
Sacher, G. A., & Staffeldt, E. F. (1974) · The American Naturalist · doi:10.1086/282938 · Cited by 451 · see citing works
Evolutionary theory of parent–offspring conflict
Godfray, H. C. J. (1995) · Nature · doi:10.1038/376133a0 · Cited by 428 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., Anderson, N. F., Dean, W., Ferguson‐Smith, A. C., Tycko, B., & Sibley, C. P. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00035.x · Cited by 409 · see citing works
Evolution of the mammalian placenta revealed by phylogenetic analysis
Wildman, D. E., Chen, C., Erez, O., Grossman, L. I., Goodman, M., & Romero, R. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511344103 · Cited by 341 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., et al. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033274 · Cited by 315 · see citing works
Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development
Redmer, D. A., Wallace, J. M., & Reynolds, L. P. (2004) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2004.06.006 · Cited by 294 · see citing works
Parent‐Offspring Conflict in the Evolution of Vertebrate Reproductive Mode
Crespi, B. J., & Semeniuk, C. A. D. (2004) · The American Naturalist · doi:10.1086/382734 · Cited by 279 · see citing works
Comparative aspects of trophoblast development and placentation
Carter, A. M., & Enders, A. C. (2004) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-2-46 · Cited by 255 · see citing works
Comparative Placentation: Structures, Functions and Evolution
Wooding, P., & Burton, G. (2008) · doi:10.1007/978-3-540-78797-6 · Cited by 228 · see citing works
Allen, W. R., Wilsher, S., Turnbull, C., Stewart, F., Ousey, J., Rossdale, P. D., & Fowden, A. L. (2002) · Reproduction · doi:10.1530/rep.0.1230445 · Cited by 223 · see citing works
Regulation of Placental Efficiency for Nutrient Transport by Imprinted Genes
Angiolini, E., Fowden, A., Coan, P., Sandovici, I., Smith, P., Dean, W., Burton, G., Tycko, B., Reik, W., Sibley, C., et al. (2006) · Placenta · doi:10.1016/j.placenta.2005.12.008 · Cited by 179 · see citing works
Mess, A., & Carter, A. M. (2005) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21079 · Cited by 174 · see citing works
Hradecký, P., & Mossman, H. W. (1987) · The Journal of Zoo Animal Medicine · doi:10.2307/20460238 · Cited by 163 · see citing works
The marsupial placenta: A phylogenetic analysis
Freyer, C., Zeller, U., & Renfree, M. B. (2003) · Journal of Experimental Zoology Part A Comparative Experimental Biology · doi:10.1002/jez.a.10291 · Cited by 137 · see citing works
Review: Marsupials: Placental Mammals with a Difference
Renfree, M. B. (2010) · Placenta · doi:10.1016/j.placenta.2009.12.023 · Cited by 129 · see citing works
The mammalian yolk sac placenta
Freyer, C., & Renfree, M. B. (2008) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21239 · Cited by 127 · see citing works
Roberts, C. T., Sohlström, A., Kind, K. L., Earl, R., Khong, T. Y., Robinson, J. S., Owens, P. C., & Owens, J. A. (2001) · Placenta · doi:10.1053/plac.2000.0602 · Cited by 124 · see citing works
Phylogenetic Evidence for Early Hemochorial Placentation in Eutheria
Elliot, M. G., & Crespi, B. J. (2009) · Placenta · doi:10.1016/j.placenta.2009.08.004 · Cited by 121 · see citing works
Vogel, P. (2005) · Placenta · doi:10.1016/j.placenta.2004.11.005 · Cited by 114 · see citing works
Evolution of the placenta during the early radiation of placental mammals
Mess, A., & Carter, A. M. (2007) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2007.01.029 · Cited by 96 · see citing works
Parent–Offspring Conflict in Primates
Maestripieri, D. (2002) · International Journal of Primatology · doi:10.1023/a:1015537201184 · Cited by 95 · see citing works
Changes in Placental Size during Ramadan
Alwasel, S. H., Abotalib, Z., Aljarallah, J. S., Osmond, C., Alkharaz, S. M., Alhazza, I. M., Badr, G., & Barker, D. J. P. (2010) · Placenta · doi:10.1016/j.placenta.2010.04.010 · Cited by 92 · see citing works
Unearthing the Roles of Imprinted Genes in the Placenta
Bressan, F. F., De, T. H. C., Perecin, F., Lopes, F. L., Ambrósio, C. E., Meirelles, F. V., & Miglino, M. (2009) · Placenta · doi:10.1016/j.placenta.2009.07.007 · Cited by 89 · see citing works
Effects of famine on placental size and efficiency
Roseboom, T. J., Painter, R. C., de Rooij, S. R., van Abeelen, A. F. M., Veenendaal, M. V. E., Osmond, C., & Barker, D. J. P. (2011) · Placenta · doi:10.1016/j.placenta.2011.03.001 · Cited by 84 · see citing works
Placentation and Maternal Investment in Mammals
Capellini, I., Venditti, C., & Barton, R. A. (2011) · The American Naturalist · doi:10.1086/657435 · Cited by 81 · see citing works
Self-citationDoes the fetal genotype affect maternal physiology during pregnancy?
Petry, C. J., Ong, K. K., & Dunger, D. B. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.07.007 · Cited by 79 · see citing works
Evolution of the Placenta and Fetal Membranes Seen in the Light of Molecular Phylogenetics
Carter, A. M. (2001) · Placenta · doi:10.1053/plac.2001.0739 · Cited by 79 · see citing works
Period of gestation and body weight in some placental mammals
Kihlström, J. E. (1972) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(72)90254-x · Cited by 64 · see citing works
Genomic Imprinting as a Mechanism of Reproductive Isolation in Mammals
Vrana, P. B. (2007) · Journal of Mammalogy · doi:10.1644/06-mamm-s-013r1.1 · Cited by 63 · see citing works
Evolution of Placentation in Primates: Implications of Mammalian Phylogeny
Martin, R. D. (2008) · Evolutionary Biology · doi:10.1007/s11692-008-9016-9 · Cited by 62 · see citing works
Evolution of Factors Affecting Placental Oxygen Transfer
Carter, A. M. (2008) · Placenta · doi:10.1016/j.placenta.2008.11.006 · Cited by 60 · see citing works
Life history consequences of mammal sibling rivalry
Stockley, P., & Parker, G. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192125999 · Cited by 58 · see citing works
Luckett, P. (1976) · Folia Primatologica · doi:10.1159/000155719 · Cited by 57 · see citing works
Klisch, K., & Mess, A. (2006) · Placenta · doi:10.1016/j.placenta.2006.03.014 · Cited by 54 · see citing works
Physiology of Placental Transfer in Mammals
Faber, J. J., Thornburg, K. L. R., & Binder, N. D. (1992) · American Zoologist · doi:10.1093/icb/32.2.343 · Cited by 48 · see citing works
Schlabritz‐Loutsevitch, N., Ballesteros, B., Dudley, C., Jenkins, S. L., Hubbard, G. B., Burton, G. J., & Nathanielsz, P. W. (2007) · Placenta · doi:10.1016/j.placenta.2006.11.012 · Cited by 45 · see citing works
Placental invasiveness and brain–body allometry in eutherian mammals
Elliot, M. G., & Crespi, B. J. (2008) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2008.01590.x · Cited by 43 · see citing works
The evolving placenta: Convergent evolution of variations in the endotheliochorial relationship
Enders, A. C., & Carter, A. M. (2012) · Placenta · doi:10.1016/j.placenta.2012.02.008 · Cited by 41 · see citing works
Review: Parent-offspring conflict and the control of placental function
Moore, T. (2011) · Placenta · doi:10.1016/j.placenta.2011.11.016 · Cited by 40 · see citing works
Placentation in the alpaca Lama pacos
Olivera, L., Zago, D., Leiser, R., Jones, C. J. P., & Bevilacqua, E. M. A. F. (2003) · Anatomy and Embryology · doi:10.1007/s00429-003-0328-3 · Cited by 35 · see citing works
Ng, H., Novakovic, B., Hiendleder, S., Craig, J. M., Roberts, C. T., & Saffery, R. (2010) · Placenta · doi:10.1016/j.placenta.2010.01.009 · Cited by 33 · see citing works
Weaning in the guinea pig (Cavia aperea f. porcellus): Who decides and by what measure?
Rehling, A., & Trillmich, F. (2007) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-007-0449-4 · Cited by 33 · see citing works
Rutherford, J. N., & Tardif, S. D. (2008) · Placenta · doi:10.1016/j.placenta.2008.10.010 · Cited by 32 · see citing works
Developmental changes in localization of steroid synthesis enzymes in camelid placenta
Wooding, F. B. P., Ozturk, M., Skidmore, J., et al. (2003) · Reproduction · doi:10.1530/rep.0.1260239 · Cited by 29 · see citing works
Marsupials: Placental Mammals with a Difference
Renfree, M. B. (2010) · Placenta · Cited by 29 · see citing works
Mother–offspring conflict in captive plains zebra (Equus burchellii): Suckling bout duration
Pluháček, J., Bartoš, L., & Bartošová, J. (2010) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2009.11.009 · Cited by 21 · see citing works
Haeckel, E. (1903) · W. Engelmann eBooks · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
A review of inter- and intraspecific variation in the eutherian placenta
Gundling, W. E., & Wildman, D. E. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0072 · Cited by 58 · see citing works
- Authors
- Capellini, I.
- Affiliations
- University of Hull (GB)
- Corresponding author
- Capellini, I.
- ORCID
- Capellini, I.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2012-10
- Volume
- 33
- Issue
- 10
- Pages
- 763-768
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W2071428783
- Cited by
- 42
- References
- 55
- Citations by year
- 2026: 1 · 2024: 5 · 2023: 5 · 2022: 2 · 2021: 1 · 2020: 1 · 2019: 3 · 2018: 3 · 2017: 3 · 2016: 6 · 2015: 6 · 2014: 2 · 2013: 3 · 2012: 1
- FWCI
- 4.62
- Type
- journal article
- Language
- en
- Open access
- Licence
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Repository@Hull (Worktribe) (University of Hull) (acceptedVersion, other-oa)
- Repository@Hull (Worktribe) (University of Hull) (submittedVersion, cc-by)
- Research Portal (Queen's University Belfast) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/E014593/1)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- placental morphology, fetal growth rate, gestation length, maternal investment, placental evolution, neonate size
- MeSH terms
- Animals, Female, Humans, Maternal-Fetal Exchange, Placentation, Pregnancy, Reproduction, Trophoblasts, Placental Circulation, Fetal Development
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
