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Reuse of homologous genes during the evolution of similar traits or ecological transitions is often taken as evidence that evolution is repeatable at the molecular level. To study gene reuse, biologists frequently select specific convergent phenotypes and search for signatures of natural selection in genomes associated with those phenotypes. However, the causes and frequency of genome-scale molecular convergence remain unresolved, especially over deep timescales. We use phylotranscriptomics and analyses of sequence evolution to show that adaptive molecular convergence—defined as excess convergence of nonsynonymous substitutions between homologs, consistent with positive selection—is widespread across Medusozoa. Molecular convergence declines slightly over time but persists among lineages separated by over 600 My, consistently exceeding null expectations based on random overlap. Moreover, lineages sharing repeatedly evolved phenotypes (eyes, medusa loss, and upright colonies) do not exhibit elevated molecular convergence relative to other comparisons. Instead, convergence occurs idiosyncratically among species pairs and is broadly concentrated in genes associated with environment-facing functions, including metabolism, immunity, and xenobiotic processing. Our results suggest that selection often drives similar protein substitutions in disparate lineages, but that the selective causes of molecular convergence reflect multifaceted, lineage-specific interactions between organisms and their environments.
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Genomic Basis of Convergent Island Phenotypes in Boa Constrictors
Abstract Convergent evolution is often documented in organisms inhabiting isolated environments with distinct ecological conditions and similar selective regimes. Several Central America islands harbor dwarf Boa populations that are characterized by distinct differences in growth, mass, and craniofacial morphology, which are linked to the shared arboreal and feast-famine ecology of these island populations. Using high-density RADseq data, we inferred three dwarf island populations with independent origins and demonstrate that selection, along with genetic drift, has produced both divergent and convergent molecular evolution across island populations. Leveraging whole-genome resequencing data for 20 individuals and a newly annotated Boa genome, we identify four genes with evidence of phenotypically relevant protein-coding variation that differentiate island and mainland populations. The known roles of these genes involved in body growth (PTPRS, DMGDH, and ARSB), circulating fat and cholesterol levels (MYLIP), and craniofacial development (DMGDH and ARSB) in mammals link patterns of molecular evolution with the unique phenotypes of these island forms. Our results provide an important genome-wide example for quantifying expectations of selection and convergence in closely related populations. We also find evidence at several genomic loci that selection may be a prominent force of evolutionary change—even for small island populations for which drift is predicted to dominate. Overall, while phenotypically convergent island populations show relatively few loci under strong selection, infrequent patterns of molecular convergence are still apparent and implicate genes with strong connections to convergent phenotypes.
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- PAR ID:
- 10134626
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 11
- Issue:
- 11
- ISSN:
- 1759-6653
- Page Range / eLocation ID:
- 3123 to 3143
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/gbe/evz226
