Abstract
How the neural structures supporting human cognition developed and arose in evolution is an enduring question of interest. Yet, we still lack appropriate procedures to align ages across primates, and this lacuna has hindered progress in understanding the evolution of biological programs. We generated a dataset of unprecedented size consisting of 573 time points from abrupt and gradual changes in behavior, anatomy, and transcription across human and 8 nonhuman primate species. We included time points from diverse human populations to capture within-species variation in the generation of cross-species age alignments. We also extracted corresponding ages from organoids. The identification of corresponding ages across the lifespan of 8 primate species, including apes (e.g., orangutans, gorillas) and monkeys (i.e., marmosets, macaques), reveals that some biological pathways are extended in humans compared with some nonhuman primates. Notably, the human lifespan is unusually extended relative to studied nonhuman primates demonstrating that very old age is a phase of life in humans that does not map to other studied primate species. More generally, our work prompts a reevaluation in the choice of a model system to understand aging given very old age in humans is a period of life without a clear counterpart in great apes.
| Original language | English |
|---|---|
| Article number | pgad230 |
| Pages (from-to) | 1-13 |
| Journal | PNAS Nexus |
| Volume | 2 |
| Issue number | 8 |
| Early online date | 20 Jul 2023 |
| DOIs | |
| Publication status | Published - 1 Aug 2023 |
Data Availability Statement
Data are in the supplementary tables. Scripts are available onDryad: (DOI: 10.5061/dryad.0cfxpnw7r). We obtained radiograph
images from the North Carolina Zoo (contact email: research@
nczoo.org). Further access to these data beyond supplied in the
present study may require approval by the North Carolina Zoo.
Acknowledgements
We thank Emily Lynch for access to radiographs. Some data arefrom the Allen Institute and the Brainspan Atlas of the developing
human brain (http://www.brainspan.org; http://developingmouse.
brain-map.org). The acquisition of some data were supported by
the National Institutes of Health (NIH) Contract HHSN-271-
2008-00 047-C. Some scans are from the Digital Morphology
Museum, Kyoto University Primate Research Institute (KUPRI).
This research made use of the Primate Aging Database (https://
primatedatabase.org/), which is an initiative of the National
Institute on Aging. We thank Christine Vincent for quality control
and Javier Lazzaro for drawings, some of which were created with
BioRender.com. An earlier version of this manuscript was posted
as a preprint: https://doi.org/10.1101/2022.10.28.513899.
Funding
This work was supported by an INBRE pilot grant from NIGMS (P20GM103446) to [C.J.C], an R21 from NICHD (R21HD101964) to [C.J.C], a NIGMS COBRE (5P20GM103653), and start-up funds from Auburn University. BARD is supported by UK Research and Innovation (UKRI), grant number EP/S023437/1, belonging to the UKRI CDT in Accountable, Responsible and Transparent Artificial Intelligence. These opinions are not necessarily those of the NIH. Some of these data are from the national chimpanzee brain resource (NS092988) and from OASIS: Longitudinal: P50 AG05681, P01 AG03991, P01 AG026276, R01 AG021910, P20 MH071616, U24 RR021382.
ASJC Scopus subject areas
- General
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