Evolutionary Patterns of Maternal Recognition of Pregnancy and Implantation in Eutherian Mammals

Overview

Journal Animals (Basel)

Date 2024 Jul 27

PMID 39061539

Authors

Henrique Bartolomeu Braz

Rodrigo da Silva Nunes Barreto

Leandro Norberto da Silva-Junior

Bianca de Oliveira Horvath-Pereira

Thamires Santos da Silva

Monica Duarte da Silva

Francisco Acuna

Maria Angelica Miglino

Affiliations

Soon will be listed here.

Abstract

The implantation of the embryo into the maternal endometrium is a complex process associated with the evolution of viviparity and placentation in mammals. In this review, we provide an overview of maternal recognition of pregnancy signals and implantation modes in eutherians, focusing on their diverse mechanisms and evolutionary patterns. Different pregnancy recognition signals and implantation modes have evolved in eutherian mammals, reflecting the remarkable diversity of specializations in mammals following the evolution of viviparity. Superficial implantation is the ancestral implantation mode in Eutheria and its major clades. The other modes, secondary, partially, and primary interstitial implantation have each independently evolved multiple times in the evolutionary history of eutherians. Although significant progress has been made in understanding pregnancy recognition signals and implantation modes, there is still much to uncover. Rodents and chiropterans (especially Phyllostomidae) offer valuable opportunities for studying the transitions among implantation modes, but data is still scarce for these diverse orders. Further research should focus on unstudied taxa so we can establish robust patterns of evolutionary changes in pregnancy recognition signaling and implantation modes.

References

Blackburn D . Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis. J Morphol. 2014; 276(8):961-90. DOI: 10.1002/jmor.20272. View

Bianchi C, Gallelli M, Herrera J, Benavente M, Rossetto L, Aba M . Current knowledge about the processes of luteolysis and maternal recognition of pregnancy in camelids. Reprod Domest Anim. 2022; 58(1):3-9. DOI: 10.1111/rda.14269. View

Seshagiri P, Sen Roy S, Sireesha G, Rao R . Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol. 2009; 83(1-2):79-84. DOI: 10.1016/j.jri.2009.06.264. View

Luckett W, MOSSMAN H . Development and phylogenetic significance of the fetal membranes and placenta of the African hystricognathous rodents Bathyergus and Hystrix. Am J Anat. 1981; 162(3):265-85. DOI: 10.1002/aja.1001620307. View

Renfree M . Review: Marsupials: placental mammals with a difference. Placenta. 2010; 31 Suppl:S21-6. DOI: 10.1016/j.placenta.2009.12.023. View

Mayor P, Guimaraes D, Lopez-Bejar M . Progesterone and estradiol-17β as a potential method for pregnancy diagnosis in the collared peccary (Pecari tajacu). Res Vet Sci. 2012; 93(3):1413-7. DOI: 10.1016/j.rvsc.2012.04.006. View

Carter A, Mess A . Evolution of the placenta and associated reproductive characters in bats. J Exp Zool B Mol Dev Evol. 2008; 310(5):428-49. DOI: 10.1002/jez.b.21216. View

Oduor-Okelo D, Katema R, Carter A . Placenta and fetal membranes of the four-toed elephant shrew, Petrodromus tetradactylus. Placenta. 2004; 25(10):803-9. DOI: 10.1016/j.placenta.2004.03.001. View

Paulson E, Comizzoli P . Endometrial receptivity and embryo implantation in carnivores-commonalities and differences with other mammalian species. Biol Reprod. 2021; 104(4):771-783. DOI: 10.1093/biolre/ioab001. View

10.

MOSSMAN H . Classics revisited: Comparative morphogenesis of the fetal membranes and accessory uterine structures. Placenta. 1991; 12(1):1-5. DOI: 10.1016/0143-4004(91)90504-9. View

11.

Bazer F . Pregnancy recognition signaling mechanisms in ruminants and pigs. J Anim Sci Biotechnol. 2013; 4(1):23. PMC: 3710217. DOI: 10.1186/2049-1891-4-23. View

12.

Oduor-Okelo D . Histology of the chorioallantoic placenta of the golden-rumped elephant shrew (Rhynchocyon chrysopygus Gunther, 1881). Anat Anz. 1984; 157(5):395-407. View

13.

Hao X, Lu Q, Zhao H . A molecular phylogeny for all 21 families within Chiroptera (bats). Integr Zool. 2023; 19(5):989-998. DOI: 10.1111/1749-4877.12772. View

14.

Maston G, Ruvolo M . Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection. Mol Biol Evol. 2002; 19(3):320-35. DOI: 10.1093/oxfordjournals.molbev.a004085. View

15.

Kimura K, Uchida T . Ultrastructural observations of delayed implantation in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. J Reprod Fertil. 1983; 69(1):187-93. DOI: 10.1530/jrf.0.0690187. View

16.

Lee K, DeMayo F . Animal models of implantation. Reproduction. 2004; 128(6):679-95. DOI: 10.1530/rep.1.00340. View

17.

McGowen M, Erez O, Romero R, Wildman D . The evolution of embryo implantation. Int J Dev Biol. 2014; 58(2-4):155-61. PMC: 6053685. DOI: 10.1387/ijdb.140020dw. View

18.

Ferner K, Siniza S, Zeller U . The placentation of eulipotyphla-reconstructing a morphotype of the Mammalian placenta. J Morphol. 2014; 275(10):1122-44. DOI: 10.1002/jmor.20289. View

19.

WIMSATT W, Enders A . Structure and morphogenesis of the uterus, placenta, and paraplacental organs of the neotropical disc-winged bat Thyroptera tricolor spix (Microchiroptera: Thyropteridae). Am J Anat. 1980; 159(2):209-43. DOI: 10.1002/aja.1001590208. View

20.

Freyer C, Zeller U, Renfree M . The marsupial placenta: a phylogenetic analysis. J Exp Zool A Comp Exp Biol. 2003; 299(1):59-77. DOI: 10.1002/jez.a.10291. View