Gene Expression and Adaptive Noncoding Changes During Human Evolution

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2017 Jun 7

PMID 28583075

Citations 8

Authors

Courtney C Babbitt

Ralph Haygood

William J Nielsen

Gregory A Wray

Affiliations

Soon will be listed here.

Abstract

Background: Despite evidence for adaptive changes in both gene expression and non-protein-coding, putatively regulatory regions of the genome during human evolution, the relationship between gene expression and adaptive changes in cis-regulatory regions remains unclear.

Results: Here we present new measurements of gene expression in five tissues of humans and chimpanzees, and use them to assess this relationship. We then compare our results with previous studies of adaptive noncoding changes, analyzing correlations at the level of gene ontology groups, in order to gain statistical power to detect correlations.

Conclusions: Consistent with previous studies, we find little correlation between gene expression and adaptive noncoding changes at the level of individual genes; however, we do find significant correlations at the level of biological function ontology groups. The types of function include processes regulated by specific transcription factors, responses to genetic or chemical perturbations, and differentiation of cell types within the immune system. Among functional categories co-enriched with both differential expression and noncoding adaptation, prominent themes include cancer, particularly epithelial cancers, and neural development and function.

Citing Articles

Ecological Trait Differences Are Associated with Gene Expression in the Primary Visual Cortex of Primates.

Zintel T, Ely J, Raghanti M, Hopkins W, Hof P, Sherwood C Genes (Basel). 2025; 16(2).

PMID: 40004446 PMC: 11855002. DOI: 10.3390/genes16020117.

A molecular and cellular perspective on human brain evolution and tempo.

Lindhout F, Krienen F, Pollard K, Lancaster M Nature. 2024; 630(8017):596-608.

PMID: 38898293 DOI: 10.1038/s41586-024-07521-x.

Evolution and dysfunction of human cognitive and social traits: A transcriptional regulation perspective.

Zug R, Uller T Evol Hum Sci. 2023; 4:e43.

PMID: 37588924 PMC: 10426018. DOI: 10.1017/ehs.2022.42.

Returning to basic principles to develop more effective treatments for central nervous system disorders.

Wexler B Exp Biol Med (Maywood). 2022; 247(10):856-867.

PMID: 35172621 PMC: 9158240. DOI: 10.1177/15353702221078291.

Adaptive eQTLs reveal the evolutionary impacts of pleiotropy and tissue-specificity while contributing to health and disease.

Quiver M, Lachance J HGG Adv. 2022; 3(1):100083.

PMID: 35047867 PMC: 8756519. DOI: 10.1016/j.xhgg.2021.100083.

References

Pollard K, Salama S, King B, Kern A, Dreszer T, Katzman S . Forces shaping the fastest evolving regions in the human genome. PLoS Genet. 2006; 2(10):e168. PMC: 1599772. DOI: 10.1371/journal.pgen.0020168. View

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

Subramanian A, Tamayo P, Mootha V, Mukherjee S, Ebert B, Gillette M . Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102(43):15545-50. PMC: 1239896. DOI: 10.1073/pnas.0506580102. View

Lein E, Hawrylycz M, Ao N, Ayres M, Bensinger A, Bernard A . Genome-wide atlas of gene expression in the adult mouse brain. Nature. 2006; 445(7124):168-76. DOI: 10.1038/nature05453. View

Blekhman R, Marioni J, Zumbo P, Stephens M, Gilad Y . Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 2009; 20(2):180-9. PMC: 2813474. DOI: 10.1101/gr.099226.109. View

Grundberg E, Small K, Hedman A, Nica A, Buil A, Keildson S . Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat Genet. 2012; 44(10):1084-9. PMC: 3784328. DOI: 10.1038/ng.2394. View

Han M, Demuth J, McGrath C, Casola C, Hahn M . Adaptive evolution of young gene duplicates in mammals. Genome Res. 2009; 19(5):859-67. PMC: 2675974. DOI: 10.1101/gr.085951.108. View

Wray G . The evolutionary significance of cis-regulatory mutations. Nat Rev Genet. 2007; 8(3):206-16. DOI: 10.1038/nrg2063. View

Robinson M, McCarthy D, Smyth G . edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009; 26(1):139-40. PMC: 2796818. DOI: 10.1093/bioinformatics/btp616. View

10.

Wierstra I . The transcription factor FOXM1 (Forkhead box M1): proliferation-specific expression, transcription factor function, target genes, mouse models, and normal biological roles. Adv Cancer Res. 2013; 118:97-398. DOI: 10.1016/B978-0-12-407173-5.00004-2. View

11.

Haygood R, Babbitt C, Fedrigo O, Wray G . Contrasts between adaptive coding and noncoding changes during human evolution. Proc Natl Acad Sci U S A. 2010; 107(17):7853-7. PMC: 2867918. DOI: 10.1073/pnas.0911249107. View

12.

Abecasis G, Auton A, Brooks L, DePristo M, Durbin R, Handsaker R . An integrated map of genetic variation from 1,092 human genomes. Nature. 2012; 491(7422):56-65. PMC: 3498066. DOI: 10.1038/nature11632. View

13.

Carroll S . Evolution at two levels: on genes and form. PLoS Biol. 2005; 3(7):e245. PMC: 1174822. DOI: 10.1371/journal.pbio.0030245. View

14.

Liberzon A . A description of the Molecular Signatures Database (MSigDB) Web site. Methods Mol Biol. 2014; 1150:153-60. DOI: 10.1007/978-1-4939-0512-6_9. View

15.

. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2016; 45(D1):D158-D169. PMC: 5210571. DOI: 10.1093/nar/gkw1099. View

16.

Enard D, Messer P, Petrov D . Genome-wide signals of positive selection in human evolution. Genome Res. 2014; 24(6):885-95. PMC: 4032853. DOI: 10.1101/gr.164822.113. View

17.

McClure H . Tumors in nonhuman primates: observations during a six-year period in the Yerkes primate center colony. Am J Phys Anthropol. 1973; 38(2):425-9. DOI: 10.1002/ajpa.1330380243. View

18.

Gilad Y, Mizrahi-Man O . A reanalysis of mouse ENCODE comparative gene expression data. F1000Res. 2015; 4:121. PMC: 4516019. DOI: 10.12688/f1000research.6536.1. View

19.

Kosiol C, Vinar T, da Fonseca R, Hubisz M, Bustamante C, Nielsen R . Patterns of positive selection in six Mammalian genomes. PLoS Genet. 2008; 4(8):e1000144. PMC: 2483296. DOI: 10.1371/journal.pgen.1000144. View

20.

Liberzon A, Birger C, Thorvaldsdottir H, Ghandi M, Mesirov J, Tamayo P . The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 2016; 1(6):417-425. PMC: 4707969. DOI: 10.1016/j.cels.2015.12.004. View