Abstract
Embryonic development in nonmammalian vertebrates depends entirely on nutritional reserves that are predominantly derived from vitellogenin proteins and stored in egg yolk. Mammals have evolved new resources, such as lactation and placentation, to nourish their developing and early offspring. However, the evolutionary timing and molecular events associated with this major phenotypic transition are not known. By means of sensitive comparative genomics analyses and evolutionary simulations, we here show that the three ancestral vitellogenin-encoding genes were progressively lost during mammalian evolution (until around 30–70 million years ago, Mya) in all but the egg-laying monotremes, which have retained a functional vitellogenin gene. Our analyses also provide evidence that the major milk resource genes, caseins, which have similar functional properties as vitellogenins, appeared in the common mammalian ancestor ∼200–310 Mya. Together, our data are compatible with the hypothesis that the emergence of lactation in the common mammalian ancestor and the development of placentation in eutherian and marsupial mammals allowed for the gradual loss of yolk-dependent nourishment during mammalian evolution.
Highlights
Nutritional reserves that are stored in egg yolk are crucial for the development of the embryo of nonmammalian oviparous vertebrates [1]
Using detailed evolutionary analyses of genomes from the three major mammalian lineages, we found that these genes progressively lost their functions and became pseudogenes relatively recently during mammalian evolution
We suggest that the emergence of the alternative resources for the mammalian young—lactation and placentation—only gradually reduced the need for egg yolk resources in mammals
Summary
Nutritional reserves that are stored in egg yolk are crucial for the development of the embryo of nonmammalian oviparous vertebrates [1]. In the extant egg-laying (oviparous) species that are closest to mammals—reptiles and birds—the composition of yolk is well known [1,2]. It mainly consists of proteins, lipids, phosphorous, and calcium, most of which are either contained in or transported to the egg by vitellogenin (VTG), which is produced in the liver. Monotremes (prototherians) are the only extant oviparous mammalian species (Figure 1) They possess mammary glands like marsupials and eutherians, but teats are absent and milk is supplied to the offspring by leakage onto the abdominal milk patch [4].
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