Hundreds of genes experienced convergent shifts in selective pressure in marine mammals
Open accessAbstract
Mammal species have made the transition to the marine environment several times, and their lineages represent one of the classical examples of convergent evolution in morphological and physiological traits. Nevertheless, the genetic mechanisms of their phenotypic transition are poorly understood, and investigations into convergence at the molecular level have been inconclusive. While past studies have searched for convergent changes at specific amino acid sites, we propose an alternative strategy to identify those genes that experienced convergent changes in their selective pressures, visible as changes in evolutionary rate specifically in the marine lineages. We present evidence of widespread convergence at the gene level by identifying parallel shifts in evolutionary rate during three independent episodes of mammalian adaptation to the marine environment. Hundreds of genes accelerated their evolutionary rates in all three marine mammal lineages during their transition to aquatic life. These marine-accelerated genes are highly enriched for pathways that control recognized functional adaptations in marine mammals, including muscle physiology, lipid-metabolism, sensory systems, and skin and connective tissue. The accelerations resulted from both adaptive evolution as seen in skin and lung genes, and loss of function as in gustatory and olfactory genes. In regard to sensory systems, this finding provides further evidence that reduced senses of taste and smell are ubiquitous in marine mammals. Our analysis demonstrates the feasibility of identifying genes underlying convergent organism-level characteristics on a genome-wide scale and without prior knowledge of adaptations, and provides a powerful approach for investigating the physiological functions of mammalian genes.
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Desmocollin and desmoglein genes have expanded in the tetrapods, and desmosome genes are subject to selection during re-invasion of aquatic environments in mammals.
“Desmocollin and desmoglein genes have expanded in the tetrapods (Green et al., 2020) and desmosome genes are subject to selection during re-invasion of aquatic environments in mammals (Chikina et al., 2016)”
From Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish (2020) · cites this paper as Chikina et al., 2016
Convergent rate changes can arise via consistent shifts in substitution rate in genomic regions influencing particular phenotypic targets of natural selection.
“Convergence at the molecular level can arise because of identical substitutions, and convergent rate changes can arise via consistent shifts in substitution rate in genomic regions influencing particular phenotypic targets of natural selection”
From Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees (2019) · cites this paper as Chikina et al. 2016
Chikina et al. quantified the difference of relative substitution rates between terrestrial and marine branches using a nonparametric test (Wilcoxon rank sum test); the same approach has been extended to noncoding regions.
“Chikina et al. (2016), studying protein-coding genes with convergent substitution rate shifts in marine mammals, quantified the difference of relative substitution rates between “terrestrial” and “marine” branches using a nonparametric test (Wilcoxon rank sum test); the same approach has subsequently been extended to noncoding regions (Partha et al. 2017).”
From Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees (2019) · cites this paper as Chikina et al. 2016
Convergence at the molecular level can arise because of identical substitutions.
“Convergence at the molecular level can arise because of identical substitutions, and convergent rate changes can arise via consistent shifts in substitution rate in genomic regions influencing particular phenotypic targets of natural selection”
From Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees (2019) · cites this paper as Chikina et al. 2016
The P-values of both the likelihood ratio test and Wilcoxon rank sum test cannot distinguish between convergent acceleration in all target species (case 7) and slight acceleration in all ratites and tinamous (case 8) or acceleration in only one lineage (case 3).
“But the P-values of both likelihood ratio test and Wilcoxon rank sum test cannot distinguish between this pattern and one in which all ratites and tinamous are slightly accelerated (case 8) or in which only one lineage is accelerated (case 3).”
From Bayesian Detection of Convergent Rate Changes of Conserved Noncoding Elements on Phylogenetic Trees (2019) · cites this paper as Chikina et al. 2016
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- Authors
- Chikina, M., Robinson, J. D., & Clark, N. L.
- Affiliations
- University of Pittsburgh (US)
- University of California, Berkeley (US)
- Corresponding author
- Chikina, Maria
- Clark, Nathan L.
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-06-21
- Volume
- 33
- Issue
- 9
- Pages
- 2182-2192
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- PMC
- PMC5854031
- OpenAlex
- W2465050739
- Cited by
- 171
- References
- 71
- Citations by year
- 2026: 20 · 2025: 15 · 2024: 13 · 2023: 18 · 2022: 16 · 2021: 18 · 2020: 23 · 2019: 29 · 2018: 10 · 2017: 6 · 2016: 2
- FWCI
- 12.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Science Foundation
- U.S. Department of Defense
- Foundation for the National Institutes of Health
- Pittsburgh Foundation
- Broad Institute
- National Human Genome Research Institute (U54HG008540)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- marine mammals, convergent evolution, adaptive evolution, loss of function, olfactory genes, sensory systems, lipid metabolism, muscle physiology
- MeSH terms
- Adaptation, Physiological, Animals, Cetacea, Biological Evolution, Phenotype, Phylogeny, Caniformia, Selection, Genetic, Evolution, Molecular, Sirenia, Aquatic Organisms, Mutation Rate, Gene-Environment Interaction
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