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Cited by 73Genetics, Aging, and Longevity in Model OrganismsEvolution and Genetic DynamicsGenomics and Phylogenetic Studies

Biological processes modulating longevity across primates: a phylogenetic genome-phenome analysis

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Muntané, Gerard, Farré, Xavier, Rodríguez, Juan Antonio, Pegueroles, Cinta, Hughes, David A, de Magalhães, João Pedro, Gabaldón, Toni, Navarro, Arcadi·2018·Molecular Biology and Evolution
DOI 10.1093/molbev/msy105PMC PMC6063263
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Abstract

Aging is a complex process affecting different species and individuals in different ways. Comparing genetic variation across species with their aging phenotypes will help understanding the molecular basis of aging and longevity. Although most studies on aging have so far focused on short-lived model organisms, recent comparisons of genomic, transcriptomic, and metabolomic data across lineages with different lifespans are unveiling molecular signatures associated with longevity. Here, we examine the relationship between genomic variation and maximum lifespan across primate species. We used two different approaches. First, we searched for parallel amino-acid mutations that co-occur with increases in longevity across the primate linage. Twenty-five such amino-acid variants were identified, several of which have been previously reported by studies with different experimental setups and in different model organisms. The genes harboring these mutations are mainly enriched in functional categories such as wound healing, blood coagulation, and cardiovascular disorders. We demonstrate that these pathways are highly enriched for pleiotropic effects, as predicted by the antagonistic pleiotropy theory of aging. A second approach was focused on changes in rates of protein evolution across the primate phylogeny. Using the phylogenetic generalized least squares, we show that some genes exhibit strong correlations between their evolutionary rates and longevity-associated traits. These include genes in the Sphingosine 1-phosphate pathway, PI3K signaling, and the Thrombin/protease-activated receptor pathway, among other cardiovascular processes. Together, these results shed light into human senescence patterns and underscore the power of comparative genomics to identify pathways related to aging and longevity.

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  • 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 Muntané et al. 2018

    The Introduction (Fig. 1; page unavailable) describes testing whether gene-specific rates of protein evolution coevolve with life-history traits, and the Discussion (Limitations of the Present Study; page unavailable) describes consistent changes in protein evolution alongside changes in those traits. These passages support the idea of consistent rate–phenotype relationships, but they do not establish that natural selection on particular phenotypic targets caused the rate shifts. (LLM, conf=0.80)

    Experimental — accuracy not yet measured

  • 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 Muntané et al. 2018

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Authors
Muntané, G., Farré, X., Rodríguez, J. A., Pegueroles, C., Hughes, D. A., de Magalhães, J. P., Gabaldón, T., & Navarro, A.
Affiliations
  • Consejo Superior de Investigaciones Científicas (ES)
  • Barcelona Institute of Science and Technology (ES)
  • Universitat Pompeu Fabra (ES)
  • University of Bristol (GB)
  • Integrative Genomics of Ageing Group, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool, United Kingdom
  • Institució Catalana de Recerca i Estudis Avançats (ES)
Corresponding author
  • Muntané, Gerard
  • Navarro, Arcadi
ORCID
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2018-05-21
Volume
35
Issue
8
Pages
1990-2004
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
DOI
10.1093/molbev/msy105
PMC
PMC6063263
OpenAlex
W2803666793
Cited by
73
References
7
Citations by year
2026: 4 · 2025: 10 · 2024: 4 · 2023: 7 · 2022: 8 · 2021: 18 · 2020: 12 · 2019: 10
FWCI
4.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (publishedVersion, cc-by-nc)
  • Explore Bristol Research (publishedVersion, cc-by)
  • Bristol Research (University of Bristol) (submittedVersion, cc-by)
  • Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by-nc)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion, cc-by-nc)
Funders
  • Ministerio de Ciencia e Innovación (BFU2012-38236, BFU2015-68649-P)
  • Direcció General de Recerca, Generalitat de Catalunya (2014SGR1311, 2014SGR866, 2014BP-B00157)
  • Spanish National Institute of Bioinfomatics
  • Instituto de Salud Carlos III (PT13/0001/0026)
  • MINECO (MDM-2014-0370)
  • Fondo Europeo de Desarrollo Regional
  • Fondo Social Europeo
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
aging, longevity, maximum lifespan, primates, antagonistic pleiotropy, protein evolution rate, PI3K signaling, wound healing, coagulation, cardiovascular disease, comparative genomics
MeSH terms
Animals, Biological Evolution, Female, Humans, Longevity, Mutation, Primates, Genetic Pleiotropy

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