Uterine and Placental Angiogenesis in the Australian Skinks, Ctenotus taeniolatus, and Saiphos equalis

Abstract

The evolution of viviparity requires modifications to multiple integrated physiological features to support embryonic development during pregnancy. Embryonic growth during pregnancy is dependent upon the capacity of the uterine vascular system to satisfy increasing embryonic oxygen demand throughout gestation. We tested the hypothesis that total surface area of uterine blood vessels increases in concert with embryonic growth, and hence its oxygen demand, during gestation. We used immunofluorescence and laser-scanning confocal microscopy to quantify uterine microvascular density and morphology during gestation in the oviparous skink Ctenotus taeniolatus and in Saiphos equalis, a skink species with prolonged egg retention. For C. taeniolatus, vessel density (Nv) and vessel length-density (Lv) in the embryonic hemisphere of the uterus is 23% and 17% less, respectively, than that of S. equalis and vascular surface-area does not differ as a function of embryo stage. For S. equalis, overall Nv, Lv, and vessel diameter (Dv), does not change during the first half of gestation but increases by 36% (Nv), 44% (Lv), and 60% (Dv) by near-term embryo stages late in gestation. The chorioallantoic membrane of S. equalis increases in absolute size but vascular density does not differ as a function of embryo stage. The marked increase in uterine vascular density during late gestation coincides with the phase of rapid growth in embryo mass and concomitant increase in metabolic rate. Expansion of the uterine vascular bed in concert with embryo size and metabolism is likely to be an important transitional step in the evolution of viviparity. Anat Rec,

The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes

“…In viviparous skinks, uterine capillary density increases as embryonic mass and oxygen demand R18 J U Van Dyke and others increase , Parker et al 2010, which suggests that embryos might influence the upregulation of uterine angiogenesis . Expression of vascular endothelial growth factors (VEGFs) increases in the uterine tissues of S. equalis and E. quoyii during pregnancy , so VEGFs are involved in the angiogenic pathway in some species ).…”

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“…After ovulation, the vitellogenic processes are rapidly down-regulated to pregestational levels (Dessauer and Fox, 1959;Garstka, et al, 1985;Bonnet et al, 1994). Thereafter, the oviduct continues to undergo extensive remodeling to provide the developing embryos with an appropriate environment for gas exchange and, in some species, to facilitate the maternal-fetal transport of varying quantities of trace nutrients (Masson and Guillette, 1987;Parker et al, 2010;Blackburn and Stewart, 2011;. Similar to patterns observed in the eggs of oviparous species, embryonic metabolism increases progressively to term, from negligible levels during early embryonic development, to substantially higher values prior to parturition (Packard et al, 1977;Robert and Thompson, 2000;Schultz et al, 2008).…”

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“…during pregnancy) are attributable to (i) embryonic metabolism and (ii) maternal metabolic demand of supporting the embryos (termed the metabolic cost of pregnancy, MCP). MCP may involve numerous maternal costs including but not limited to those associated with supplying oxygen to the fetus (Bader et al, 1959;Hytten and Leitch, 1971;Grigg and Harlow, 1981;Birchard et al, 1984;Murphy et al, 2010;Parker et al, 2010), handling fetal wastes (Clark and Sisken, 1956), and, in matrotrophic species, supplying nutrients to the embryos (Stewart and Thompson, 2000).…”