Quantitative uniqueness of human brain evolution revealed through phylogenetic comparative analysis
Abstract
While the human brain is clearly large relative to body size, less is known about the timing of brain and brain component expansion within primates and the relative magnitude of volumetric increases. Using Bayesian phylogenetic comparative methods and data for both extant and fossil species, we identified that a distinct shift in brain-body scaling occurred as hominins diverged from other primates, and again as humans and Neanderthals diverged from other hominins. Within hominins, we detected a pattern of directional and accelerating evolution towards larger brains, consistent with a positive feedback process in the evolution of the human brain. Contrary to widespread assumptions, we found that the human neocortex is not exceptionally large relative to other brain structures. Instead, our analyses revealed a single increase in relative neocortex volume at the origin of haplorrhines, and an increase in relative cerebellar volume in apes.
Data availability
All data used in our analyses are provided as supplementary material.
Article and author information
Author details
Funding
National Science Foundation (BCS-1355902)
- Charles L Nunn
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jessica C. Thompson, YALE, United States
Version history
- Received: August 22, 2018
- Accepted: January 29, 2019
- Accepted Manuscript published: January 31, 2019 (version 1)
- Version of Record published: February 18, 2019 (version 2)
Copyright
© 2019, Miller et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 7,579
- views
-
- 861
- downloads
-
- 45
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Evolutionary Biology
Studies of the starlet sea anemone provide important insights into the early evolution of the circadian clock in animals.
-
- Computational and Systems Biology
- Evolutionary Biology
As the genome encodes the information crucial for cell growth, a sizeable genomic deficiency often causes a significant decrease in growth fitness. Whether and how the decreased growth fitness caused by genome reduction could be compensated by evolution was investigated here. Experimental evolution with an Escherichia coli strain carrying a reduced genome was conducted in multiple lineages for approximately 1000 generations. The growth rate, which largely declined due to genome reduction, was considerably recovered, associated with the improved carrying capacity. Genome mutations accumulated during evolution were significantly varied across the evolutionary lineages and were randomly localized on the reduced genome. Transcriptome reorganization showed a common evolutionary direction and conserved the chromosomal periodicity, regardless of highly diversified gene categories, regulons, and pathways enriched in the differentially expressed genes. Genome mutations and transcriptome reorganization caused by evolution, which were found to be dissimilar to those caused by genome reduction, must have followed divergent mechanisms in individual evolutionary lineages. Gene network reconstruction successfully identified three gene modules functionally differentiated, which were responsible for the evolutionary changes of the reduced genome in growth fitness, genome mutation, and gene expression, respectively. The diversity in evolutionary approaches improved the growth fitness associated with the homeostatic transcriptome architecture as if the evolutionary compensation for genome reduction was like all roads leading to Rome.