Genome-scale evolution in local populations of wild chimpanzees

Abstract Analysis of genome-scale evolution has been difficult in large, endangered animals because opportunities to collect high-quality genetic samples are limited. There is a need for novel field-friendly, cost-effective genetic techniques. This study conducted an exome-wide analysis of a total o...

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Main Authors: Takashi Hayakawa, Takushi Kishida, Yasuhiro Go, Eiji Inoue, Eri Kawaguchi, Tomoyuki Aizu, Hinako Ishizaki, Atsushi Toyoda, Asao Fujiyama, Tetsuro Matsuzawa, Chie Hashimoto, Takeshi Furuichi, Kiyokazu Agata
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-84163-z
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author Takashi Hayakawa
Takushi Kishida
Yasuhiro Go
Eiji Inoue
Eri Kawaguchi
Tomoyuki Aizu
Hinako Ishizaki
Atsushi Toyoda
Asao Fujiyama
Tetsuro Matsuzawa
Chie Hashimoto
Takeshi Furuichi
Kiyokazu Agata
author_facet Takashi Hayakawa
Takushi Kishida
Yasuhiro Go
Eiji Inoue
Eri Kawaguchi
Tomoyuki Aizu
Hinako Ishizaki
Atsushi Toyoda
Asao Fujiyama
Tetsuro Matsuzawa
Chie Hashimoto
Takeshi Furuichi
Kiyokazu Agata
author_sort Takashi Hayakawa
collection DOAJ
description Abstract Analysis of genome-scale evolution has been difficult in large, endangered animals because opportunities to collect high-quality genetic samples are limited. There is a need for novel field-friendly, cost-effective genetic techniques. This study conducted an exome-wide analysis of a total of 42 chimpanzees (Pan troglodytes) across six African regions, providing insights into population discrimination techniques. Wild chimpanzee DNA was extracted noninvasively from collected fecal samples using the lysis-buffer storage method. To target genome-scale regions of host DNA, exome-capture sequencing was performed using cost-effective baits originally designed for humans (closely related to chimpanzees). Multivariate analysis effectively discriminated differences in local populations, aiding in the identification of samples’ geographical origins. Exome-wide heterozygosity was negatively correlated significantly with genome-wide nonsynonymous–synonymous substitution ratios, suggesting that mutation loads exist at the local population level. Exome sequences revealed functional diversity and protein-coding gene divergence. Segregating pseudogenes were comprehensively annotated, with many being population-specific and others shared among populations. Focusing on multicopy chemosensory receptor genes, the segregating pseudogenes OR7D4 (an olfactory receptor) and TAS2R42 (a bitter taste receptor) were shared among western and eastern chimpanzees. Overall, our analytical framework offers ecological insights into chimpanzees and may be applicable to other organisms.
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spelling doaj-art-50a28e44dc1747f7bcde723dfb4176692025-01-05T12:18:31ZengNature PortfolioScientific Reports2045-23222025-01-0115111610.1038/s41598-024-84163-zGenome-scale evolution in local populations of wild chimpanzeesTakashi Hayakawa0Takushi Kishida1Yasuhiro Go2Eiji Inoue3Eri Kawaguchi4Tomoyuki Aizu5Hinako Ishizaki6Atsushi Toyoda7Asao Fujiyama8Tetsuro Matsuzawa9Chie Hashimoto10Takeshi Furuichi11Kiyokazu Agata12Faculty of Environmental Earth Science, Hokkaido UniversityCollege of Bioresource Sciences, Nihon UniversityGraduate School of Information Science, University of HyogoFaculty of Science, Toho UniversityCenter for iPS Cell Research and Application, Kyoto UniversityDepartment of Genomics and Evolutionary Biology, National Institute of GeneticsDepartment of Genomics and Evolutionary Biology, National Institute of GeneticsDepartment of Genomics and Evolutionary Biology, National Institute of GeneticsAdvanced Genomics Center, National Institute of GeneticsDepartment of Pedagogy, Chubu Gakuin UniversityWildlife Research Center, Kyoto UniversityWildlife Research Center, Kyoto UniversityLaboratory for Regenerative Biology, National Institute for Basic BiologyAbstract Analysis of genome-scale evolution has been difficult in large, endangered animals because opportunities to collect high-quality genetic samples are limited. There is a need for novel field-friendly, cost-effective genetic techniques. This study conducted an exome-wide analysis of a total of 42 chimpanzees (Pan troglodytes) across six African regions, providing insights into population discrimination techniques. Wild chimpanzee DNA was extracted noninvasively from collected fecal samples using the lysis-buffer storage method. To target genome-scale regions of host DNA, exome-capture sequencing was performed using cost-effective baits originally designed for humans (closely related to chimpanzees). Multivariate analysis effectively discriminated differences in local populations, aiding in the identification of samples’ geographical origins. Exome-wide heterozygosity was negatively correlated significantly with genome-wide nonsynonymous–synonymous substitution ratios, suggesting that mutation loads exist at the local population level. Exome sequences revealed functional diversity and protein-coding gene divergence. Segregating pseudogenes were comprehensively annotated, with many being population-specific and others shared among populations. Focusing on multicopy chemosensory receptor genes, the segregating pseudogenes OR7D4 (an olfactory receptor) and TAS2R42 (a bitter taste receptor) were shared among western and eastern chimpanzees. Overall, our analytical framework offers ecological insights into chimpanzees and may be applicable to other organisms.https://doi.org/10.1038/s41598-024-84163-zChimpanzeeLocal populationHeterozygosityPseudogeneOlfactory receptorBitter taste receptor
spellingShingle Takashi Hayakawa
Takushi Kishida
Yasuhiro Go
Eiji Inoue
Eri Kawaguchi
Tomoyuki Aizu
Hinako Ishizaki
Atsushi Toyoda
Asao Fujiyama
Tetsuro Matsuzawa
Chie Hashimoto
Takeshi Furuichi
Kiyokazu Agata
Genome-scale evolution in local populations of wild chimpanzees
Scientific Reports
Chimpanzee
Local population
Heterozygosity
Pseudogene
Olfactory receptor
Bitter taste receptor
title Genome-scale evolution in local populations of wild chimpanzees
title_full Genome-scale evolution in local populations of wild chimpanzees
title_fullStr Genome-scale evolution in local populations of wild chimpanzees
title_full_unstemmed Genome-scale evolution in local populations of wild chimpanzees
title_short Genome-scale evolution in local populations of wild chimpanzees
title_sort genome scale evolution in local populations of wild chimpanzees
topic Chimpanzee
Local population
Heterozygosity
Pseudogene
Olfactory receptor
Bitter taste receptor
url https://doi.org/10.1038/s41598-024-84163-z
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