Most non-mammalian vertebrates produce eggs with stores of yolk platelets, to provide nutrients to the developing embryo until it can feed on its own. The amount of yolk, and its influence on morphogenetic processes such as gastrulation, vary greatly across vertebrate species, but the production and storage of yolk during oogenesis share common genes and mechanisms. The large yolk protein, vitellogenin, is produced by the maternal liver, in response to estrogen, and is transported to the ovaries via the bloodstream. Oocytes take up the vitellogenin by the process of micropinocytosis, and as the protein is packaged into yolk platelets within the oocyte, it is cleaved into lipovitellins and phosvitins. Secondary processing of these cleavage products during oocyte maturation occurs differently in various non-mammalian vertebrate species, but all, from lowly lampreys to soaring falcons, share this characteristic of a vitellogenin precursor cleaved into two smaller yolk proteins (Romano et al., 2004).
Yolk sac placenta in a marsupial (Metatheria)
From Freyer et al. (2003)
Of course, mammals evolved other mechanisms to nourish developing embryos and dependent young: lactation, which is present in egg-laying monotremes (Prototheria) and defines Class Mammalia, and the placenta, which develops differently in marsupials (Metatheria) and “placental” mammals (Eutheria). Monotremes, such as the Duck-billed Platypus, lactate by leaking milk onto an abdominal milk patch, and lay yolky eggs that are nevertheless small in proportion to body size, when compared to those of birds and reptiles. Metatheria and Eutheria differ in the types of placenta formed, specifically in the particular extraembryonic membrane component that makes contact with maternal tissues. A placenta is defined as “an apposition or fusion of fetal membranes to the uterine mucosa for physiological exchange” (Mossman, 1937). The majority of marsupial species develop a placenta from the yolk sac, whereas the definitive placenta in all eutherians develops from the chorioallantois (chorion + allantois). A shell coat surrounds the marsupial conceptus early in development; this permeable structure then ruptures, allowing direct contact between the yolk sac and the uterine epithelium (Freyer et al., 2003). In eutherians, the early yolk sac placenta (choriovitelline or trilaminar omphalopleure) is replaced or even bypassed completely by a placenta that arises from a fusion of the chorion (trophoblast-derived) and the allantois, which is derived, as is the embryo itself, from the inner cell mass of the blastocyst (Carter and Enders, 2004).
Chorioallantoic placenta in a eutherian
From Carter and Enders (2004)
A new paper by Brawand and colleagues in PLoS Biology addresses the question: When were vitellogenin yolk genes phased out in mammalian evolution, as lactation and placentation took over the duties of nourishing developing embryos and dependent young? These researchers took advantage of genomics and computational biological methods to assess vitellogenin (VIT) gene remnants and inactivation, for an extant montreme species, the Duck-billed Platypus Ornithorhyncus anatinus, three metatherian species, three eutherian species, a bird, and two amphibians. Casein milk protein gene sequences were also assessed in the platypus.
Brawand and colleagues predicted that the VIT1-VIT3 genes, present in the chicken, would have been lost in viviparous eutherian mammals, such as dogs and the humans. Indeed, similarity search algorithms revealed VIT pseudogenic coding sequence remnants within both genomes, and the shared insertion/deletions (“indels”) indicated that VIT1 inactivation occurred prior to divergence of the human and dog lineages. Moreover, analysis of the Nine-banded Armadillo (Dasypus novemcinctus) gene was consistent with VIT1 inactivation preceding separation of the superorder Xenartha, Laurasiatheria, and Euarchontoglires lineages. Moving on to VIT sequences in metatherian genomes, Brawand and colleagues discovered that VIT1-VIT3 were likely to have been present in the common avian-mammalian ancestor, and that they were inactivated before the separation of Australian and American marsupials, approximately 70 million years ago. This latter analysis was possible because of the Tammar Wallaby (Macropus eugenii) genome project; the other two metatherian species examined were the Swamp Wallaby Wallabia bicolor and the Gray Short-tailed Opossum (Monodelphis domestica).
VIT gene evolution
Brawand et al. (2008) Figure 1
The platypus, an oviparous and lactating monotreme, represents the most basal mammalian lineage, and as in the opossum, VIT1 is a pseudogene in this species. However, a gene that has characteristics of both VIT2 and VIT3 was found to be intact over its entire length, with a rate of amino acid change not significantly different from the genes of birds and amphibians, and is thus likely to be functional in the platypus. The inactivation simulations for the VIT genes in both opossum and platypus are shown below. Finally, casein milk genes, in the secretory calcium-binding phosphoprotein family, were examined in the platypus, and three putative orthologous casein genes were identified in this monotreme genome. The authors conclude that nutritive lactation, as indicated by the presence of casein genes, was the initial resource that allowed loss and inactivation of some VIT genes in the common mammalian ancestor. Placentation, particularly in eutherians, and complex lactation, characteristic of metatherians, then permitted loss of the VIT2 gene during therian evolution.
Inactivation simulations for opossum and platypus
Brawand et al. (2008) Figure 6
Carter, A.M., and Enders, A.C. (2004). Comparative aspects of trophoblast deveopment and placentation. Reprod. Biol. Endocrinol. 2, 46.
Freyer, C., Zeller, U., and Renfree, M.B. (2003). the marsupial placenta: a phylogenetic analysis. J. Exp. Zool. 299A, 59-77.
Mossman, H.W. (1937). Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Inst. Contrib. Embryol. 26, 129-246.
Romano, M., Rosanova, P., Anteo, C., and Limatola, E. (2004). Vertebrate yolk proteins: a review. Mol. Reprod. Develop. 69, 109-116.
Brawand, D., Wahli, W., Kaessmann, H. (2008). Loss of Egg Yolk Genes in Mammals and the Origin of Lactation and Placentation. PLoS Biology, 6(3), e63. DOI: 10.1371/journal.pbio.0060063