Loss of egg yolk genes in mammals and the origin of lactation and placentation
Open accessAbstract
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 approximately 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.
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Case studies investigating the fate of selected genes have uncovered associations between gene losses and several mammalian phenotypes.
“Case studies investigating the fate of selected genes uncovered associations between gene losses and several mammalian phenotypes14–16.”
From A genomics approach reveals insights into the importance of gene losses for mammalian adaptations (2018) · cites this paper as [14]
Phenotypic convergence is generally believed to be a strong signature of natural selection.
“Phenotypic convergence, in which the same function or morphology evolves multiple times independently, often due to adaption to similar environmental changes, is generally believed to be a strong signature of natural selection”
From Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees (2019) · cites this paper as Brawand et al. 2008
The Results/Discussion section on functional and disabled monotreme VIT genes reports purifying selection on a platypus gene, not phenotypic convergence. Searches for phenotypic convergence and independently evolved adaptations found no passage in our copy saying that convergence is generally a strong signature of natural selection. (LLM, conf=0.76)
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A genomics approach reveals insights into the importance of gene losses for mammalian adaptations
Sharma, V., Hecker, N., Roscito, J. G., Foerster, L., Langer, B. E., & Hiller, M. (2018) · Nature Communications · doi:10.1038/s41467-018-03667-1 · Cited by 237 · see citing works
The Evolution of Milk Casein Genes from Tooth Genes before the Origin of Mammals
Kawasaki, K., Lafont, A.-G., & Sire, J.-Y. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr020 · Cited by 115 · see citing works
Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees
Hu, Z., Sackton, T. B., Edwards, S. V., & Liu, J. S. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz049 · Cited by 69 · see citing works
- Authors
- Brawand, D., Wahli, W., & Kaessmann, H.
- Affiliations
- University of Lausanne (CH)
- Corresponding author
- Wahli, Walter
- Kaessmann, Henrik
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-03-18
- Volume
- 6
- Issue
- 3
- Pages
- e63
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC2267819
- OpenAlex
- W2141406340
- Cited by
- 156
- References
- 1
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 12 · 2023: 12 · 2022: 10 · 2021: 10 · 2020: 5 · 2019: 11 · 2018: 10 · 2017: 4 · 2016: 12 · 2015: 7 · 2014: 2 · 2013: 5 · 2012: 9
- FWCI
- 7.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- SERVAL (Université de Lausanne) (publishedVersion, other-oa)
- IRIS (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Oxford University Research Archive (ORA) (University of Oxford) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Washington University School of Medicine in St. Louis
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- egg yolk, vitellogenin, gene loss, casein, milk protein, mammalian evolution, monotremes, placental mammals, marsupials, embryo nutrition, comparative genomics, evolutionary simulation
- MeSH terms
- Animals, Base Sequence, Caseins, Chickens, Egg Yolk, Female, Lactation, Mammals, Marsupialia, Molecular Sequence Data, Monotremata, Phosphoproteins, Phylogeny, Placentation, Pregnancy, Selection, Genetic, Vitellogenins, Sequence Alignment, Genome, Evolution, Molecular, Gene Silencing, Synteny
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