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. 2020 May 22;16(1):3-17.
doi: 10.21451/1984-3143-AR2018-00145.

Evolution of placentation in cattle and antelopes

Anthony M Carter  1
Affiliations

Evolution of placentation in cattle and antelopes

Anthony M Carter. Anim Reprod. .

Abstract

Bovids have enjoyed great evolutionary success as evidenced by the large number of extant species. Several important domestic animals are from this family. They derive from both subfamilies: cattle and their kin belong to Bovinae and sheep and goats to Antilopinae. The premise of this review, therefore, is that evolution of reproduction and placentation is best understood in a context that includes antelope-like bovines and antelopes. Many key features of placentation, including hormone secretion, had evolved before bovids emerged as a distinct group. Variation nevertheless occurs. Most striking is the difference in fusion of the binucleate trophoblast cell with uterine epithelium that yields a transient trinucleate cell in bovines and many antelopes, but a more persistent syncytium in wildebeest, sheep and goat. There is considerable variation in placentome number and villus branching within the placentome. Many antelopes have right-sided implantation in a bicornuate uterus whilst others have a uterus duplex. Finally, there has been continued evolution of placental hormones with tandem duplication of PAG genes in cattle, differences in glycosylation of placental lactogen and the emergence of placental growth hormone in sheep and goats. The selection pressures driving this evolution are unknown though maternal-fetal competition for nutrients is an attractive hypothesis.

Keywords: Antilopinae; Bovidae; Bovinae; binucleate trophoblast cell; chorioallantoic placenta; domestication; fetal membranes; placental hormones; placentome; unilateral implantation.

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Conflict of interest statement

Conflict of interest statement: The author declares that he has no conflicting interest.

Figures

Figure 1
Figure 1. Relative abundance of tragulids, giraffids, cervids and bovids in different geological periods (expressed as a percentage of all ruminants) in Africa (panel a) and Eurasia (panel b). MN3 and MN4 represent zones in the Early Miocene. The difference to 100% comprises pecoran species with unknown taxonomic affiliation, species from extinct pecoran families and a negligible number of musk deer (Moschidae). Reproduced with permission from (Clauss and Roessner, 2014) © Finnish Zoological and Botanical Publishing Board 2014.
Figure 2
Figure 2. Phylogenetic tree for the two subfamilies and 12 tribes of family Bovidae. The branch order is derived from Hassanin et al. (Hassanin et al., 2012). Branch lengths are arbitrary and do not refer to a time scale.
Figure 3
Figure 3. Sections through the placentomes from sheep (Ovis aries) and blue wildebeest (Connochaetes taurinus) immunostained with a PAG antibody. (a) Sheep: the fetomaternal syncytium between trophoblast and uterine stroma is continuously stained by PAG and can best be seen around the four maternal blood vessels M1, M2, M3 and M4. The nuclei in the syncytium (arrowheads) are fairly evenly spaced. F marks fetal blood vessels; Arrows, BNC. Bar = 30 µm. (b) and (c) Blue wildebeest: as in the ewe the fetomaternal syncytium is continuously stained for PAG and separates the maternal (M) and fetal (F) tissues. Nuclei (arrowheads) are scattered randomly along the syncytium. Arrows mark the BNC. Bar = 60 µm. Reproduced from (Wooding et al., 2018) © 2018 with permission from Elsevier.
Figure 4
Figure 4. Histology of the placentome in three bovids; 6 µm sections stained with haematoxylin and eosin. A. Longitudinal section of a placentome from the common eland (Taurotragus oryx) in late gestation (M26615; eland 75 in (Hradecky et al., 1988b)). Note the branching of the villi that is typical of Subfamily Bovinae. B. Cross section of a placentome from the same animal. C. Longitudinal section of a placentome from the kob (Kobus kob) at 97 days gestation; fetal length 23.4 cm (M26812; kob 7 in (Hradecky et al., 1988b)). Note the straight villi with minimal branching known only from impala and duikers. D. Cross section of a placentome from the kob at 127 days gestation; fetal length 34.5 cm (M26814; kob 9 in (Hradecky et al., 1988b)). E. Longitudinal section of a placentome from the impala (Aepyceros melampus) in mid-gestation; fetal length 11 cm (M26463; impala 118 in (Hradecky et al., 1988b)). Extensive branching of the villi is representative of the pattern in most antelopes. F. Cross section of a placentome from the same animal. Labels: b, binucleate trophoblast cell; ca, base of caruncle; fc, fetal capillary; ms, maternal stroma; v, villus. Hradecký voucher specimens in the Harland W. Mossman Embryological Collection, University of Wisconsin Zoological Museum.
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