Adaptive archaic introgression of copy number variants and the discovery of previously unknown human genes

As they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as Neanderthals and Denisovans. The result of this genetic introgression on the recipient populations has been of considerable interest, especially in cases of selection for spec...

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Published inScience (American Association for the Advancement of Science) Vol. 366; no. 6463; p. 324
Main Authors Hsieh, PingHsun, Vollger, Mitchell R., Dang, Vy, Porubsky, David, Baker, Carl, Cantsilieris, Stuart, Hoekzema, Kendra, Lewis, Alexandra P., Munson, Katherine M., Sorensen, Melanie, Kronenberg, Zev N., Murali, Shwetha, Nelson, Bradley J., Chiatante, Giorgia, Maggiolini, Flavia Angela Maria, Blanché, Hélène, Underwood, Jason G., Antonacci, Francesca, Deleuze, Jean-François, Eichler, Evan E.
Format Journal Article
LanguageEnglish
Published United States American Association for the Advancement of Science 18.10.2019
The American Association for the Advancement of Science
Subjects
Adaptation
Amino acids
Animals
Autism
Base pairs
Biochemistry, Molecular Biology
Biological evolution
Cell cycle
Chromosome 16
Chromosome 8
Chromosome Duplication
Chromosomes
Chromosomes, Human, Pair 16 - genetics
Chromosomes, Human, Pair 8 - genetics
Clonal deletion
Copy number
Demographics
DNA Copy Number Variations
Duplication
Evidence
Evolution, Molecular
Evolutionary genetics
Gene duplication
Gene mapping
Genes
Genetic diversity
Genetic Introgression
Genetic variance
Genetics
Genome, Human
Genomes
Genomics
Haplotypes
High frequencies
Hominidae - genetics
Hominids
Homo sapiens denisova
Human populations
Humans
Immune response
Individualized Instruction
Life Sciences
Local population
Melanesia
Models, Genetic
Mountains
Mutation
Neanderthals - genetics
Nucleotides
Polymorphism, Genetic
Population
Population genetics
Populations
Positive selection
Reproduction (copying)
RESEARCH ARTICLE SUMMARY
Selection, Genetic
Signatures
Whole Genome Sequencing
Melanesia
Africa
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Abstract As they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as Neanderthals and Denisovans. The result of this genetic introgression on the recipient populations has been of considerable interest, especially in cases of selection for specific archaic genetic variants. Hsieh et al. characterized adaptive structural variants and copy number variants that are likely targets of positive selection in Melanesians. Focusing on population-specific regions of the genome that carry duplicated genes and show an excess of amino acid replacements provides evidence for one of the mechanisms by which genetic novelty can arise and result in differentiation between human genomes. Science , this issue p. eaax2083 Melanesians carry adaptive DNA variants derived from archaic hominins. Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.
AbstractList Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotidevariants, but their roles in archaic introgression and adaptation have not been systematicallyinvestigated. We show that stratified CNVs are significantly associated with signatures of positiveselection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data,we reconstruct the structure and complex evolutionary history of these polymorphisms and show thatboth encode positively selected genes absent from most human populations. Our results collectivelysuggest that large CNVs originating in archaic hominins and introgressed into modern humans haveplayed an important role in local population adaptation and represent an insufficiently studied source oflarge-scale genetic variation
Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.
Adaptive archaic hominin genesAs they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as Neanderthals and Denisovans. The result of this genetic introgression on the recipient populations has been of considerable interest, especially in cases of selection for specific archaic genetic variants. Hsieh et al. characterized adaptive structural variants and copy number variants that are likely targets of positive selection in Melanesians. Focusing on population-specific regions of the genome that carry duplicated genes and show an excess of amino acid replacements provides evidence for one of the mechanisms by which genetic novelty can arise and result in differentiation between human genomes.Science, this issue p. eaax2083INTRODUCTIONCharacterizing genetic variants underlying local adaptations in human populations is one of the central goals of evolutionary research. Most studies have focused on adaptive single-nucleotide variants that either arose as new beneficial mutations or were introduced after interbreeding with our now-extinct relatives, including Neanderthals and Denisovans. The adaptive role of copy number variants (CNVs), another well-known form of genomic variation generated through deletions or duplications that affect more base pairs in the genome, is less well understood, despite evidence that such mutations are subject to stronger selective pressures.RATIONALEThis study focuses on the discovery of introgressed and adaptive CNVs that have become enriched in specific human populations. We combine whole-genome CNV calling and population genetic inference methods to discover CNVs and then assess signals of selection after controlling for demographic history. We examine 266 publicly available modern human genomes from the Simons Genome Diversity Project and genomes of three ancient hominins—a Denisovan, a Neanderthal from the Altai Mountains in Siberia, and a Neanderthal from Croatia. We apply long-read sequencing methods to sequence-resolve complex CNVs of interest specifically in the Melanesians—an Oceanian population distributed from Papua New Guinea to as far east as the islands of Fiji and known to harbor some of the greatest amounts of Neanderthal and Denisovan ancestry.RESULTSConsistent with the hypothesis of archaic introgression outside Africa, we find a significant excess of CNV sharing between modern non-African populations and archaic hominins (P = 0.039). Among Melanesians, we observe an enrichment of CNVs with potential signals of positive selection (n = 37 CNVs), of which 19 CNVs likely introgressed from archaic hominins. We show that Melanesian-stratified CNVs are significantly associated with signals of positive selection (P = 0.0323). Many map near or within genes associated with metabolism (e.g., ACOT1 and ACOT2), development and cell cycle or signaling (e.g., TNFRSF10D and CDK11A and CDK11B), or immune response (e.g., IFNLR1). We characterize two of the largest and most complex CNVs on chromosomes 16p11.2 and 8p21.3 that introgressed from Denisovans and Neanderthals, respectively, and are absent from most other human populations. At chromosome 16p11.2, we sequence-resolve a large duplication of >383 thousand base pairs (kbp) that originated from Denisovans and introgressed into the ancestral Melanesian population 60,000 to 170,000 years ago. This large duplication occurs at high frequency (>79%) in diverse Melanesian groups, shows signatures of positive selection, and maps adjacent to Homo sapiens–specific duplications that predispose to rearrangements associated with autism. On chromosome 8p21.3, we identify a Melanesian haplotype that carries two CNVs, a ~6-kbp deletion, and a ~38-kbp duplication, with a Neanderthal origin and that introgressed into non-Africans 40,000 to 120,000 years ago. This CNV haplotype occurs at high frequency (44%) and shows signals consistent with a partial selective sweep in Melanesians. Using long-read sequencing genomic and transcriptomic data, we reconstruct the structure and complex evolutionary history for these two CNVs and discover previously undescribed duplicated genes (TNFRSF10D1, TNFRSF10D2, and NPIPB16) that show an excess of amino acid replacements consistent with the action of positive selection.CONCLUSIONOur results suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation that is absent from current reference genomes.Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.
As they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as Neanderthals and Denisovans. The result of this genetic introgression on the recipient populations has been of considerable interest, especially in cases of selection for specific archaic genetic variants. Hsieh et al. characterized adaptive structural variants and copy number variants that are likely targets of positive selection in Melanesians. Focusing on population-specific regions of the genome that carry duplicated genes and show an excess of amino acid replacements provides evidence for one of the mechanisms by which genetic novelty can arise and result in differentiation between human genomes. Science , this issue p. eaax2083 Melanesians carry adaptive DNA variants derived from archaic hominins. Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.
Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation have not been systematically investigated. We show that stratified CNVs are significantly associated with signatures of positive selection in Melanesians and provide evidence for adaptive introgression of large CNVs at chromosomes 16p11.2 and 8p21.3 from Denisovans and Neanderthals, respectively. Using long-read sequence data, we reconstruct the structure and complex evolutionary history of these polymorphisms and show that both encode positively selected genes absent from most human populations. Our results collectively suggest that large CNVs originating in archaic hominins and introgressed into modern humans have played an important role in local population adaptation and represent an insufficiently studied source of large-scale genetic variation.
Author Sorensen, Melanie
Hoekzema, Kendra
Murali, Shwetha
Munson, Katherine M.
Lewis, Alexandra P.
Nelson, Bradley J.
Dang, Vy
Chiatante, Giorgia
Eichler, Evan E.
Porubsky, David
Antonacci, Francesca
Vollger, Mitchell R.
Maggiolini, Flavia Angela Maria
Kronenberg, Zev N.
Deleuze, Jean-François
Underwood, Jason G.
Cantsilieris, Stuart
Blanché, Hélène
Hsieh, PingHsun
Baker, Carl
AuthorAffiliation 3 Dipartimento di Biologia, Università degli Studi di Bari “Aldo Moro,” Bari, Italy
1 Department of Genome Sciences, University of Washington School of Medicine, Seattle, WA, USA
2 Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA
4 Fondation Jean Dausset–Centre d’Etude du Polymorphisme Humain, Paris, France
5 Pacific Biosciences (PacBio) of California, Inc., Menlo Park, CA, USA
AuthorAffiliation_xml – name: 3 Dipartimento di Biologia, Università degli Studi di Bari “Aldo Moro,” Bari, Italy
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ContentType Journal Article
Copyright Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works
Distributed under a Creative Commons Attribution 4.0 International License
Copyright_xml – notice: Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
– notice: Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works
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P.H., M.R.V., Z.N.K., J.G.U., and E.E.E. designed and planned experiments. V.D., C.B., S.C., K.H., A.P.L., K.M.M., M.S., and J.G.U. prepared libraries and generated and analyzed sequencing data. P.H., M.R.V., V.D., Z.N.K., S.M., and B.J.N. performed variant calling and bioinformatics analyses. P.H., M.R.V., and D.P. analyzed long-read sequencing data and assembled contigs. P.H. performed population genetic and phylogenetic inferences. G.C., F.A.M.M, and F.A. generated and analyzed FISH experiment data. A.P.L., K.M.M., and J.G.U. generated Iso-Seq transcript data. K.H. performed PCR assays for CNV validations. H.B. and J.-F.D. provided Melanesian genome DNA materials. P.H. and E.E.E. wrote the manuscript.
Present address: Centre for Eye Research Australia, Department of Surgery (Ophthalmology), University of Melbourne, Royal Victorian Eye and Ear Hospital, East Melbourne, VIC, Australia.
Present address: Phase Genomics, Inc., Seattle, WA, USA.
Present address: Pacific Biosciences (PacBio) of California, Inc., Menlo Park, CA, USA.
Author contributions
ORCID 0000-0003-2115-575X
0000-0002-8651-1615
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0000-0002-1525-9707
0000-0001-8413-6498
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Snippet As they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as Neanderthals and Denisovans. The...
Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotide variants, but their roles in archaic introgression and adaptation...
Adaptive archaic hominin genesAs they migrated out of Africa and into Europe and Asia, anatomically modern humans interbred with archaic hominins, such as...
Copy number variants (CNVs) are subject to stronger selective pressure than single-nucleotidevariants, but their roles in archaic introgression and adaptation...
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StartPage 324
SubjectTerms Adaptation
Amino acids
Animals
Autism
Base pairs
Biochemistry, Molecular Biology
Biological evolution
Cell cycle
Chromosome 16
Chromosome 8
Chromosome Duplication
Chromosomes
Chromosomes, Human, Pair 16 - genetics
Chromosomes, Human, Pair 8 - genetics
Clonal deletion
Copy number
Demographics
DNA Copy Number Variations
Duplication
Evidence
Evolution, Molecular
Evolutionary genetics
Gene duplication
Gene mapping
Genes
Genetic diversity
Genetic Introgression
Genetic variance
Genetics
Genome, Human
Genomes
Genomics
Haplotypes
High frequencies
Hominidae - genetics
Hominids
Homo sapiens denisova
Human populations
Humans
Immune response
Individualized Instruction
Life Sciences
Local population
Melanesia
Models, Genetic
Mountains
Mutation
Neanderthals - genetics
Nucleotides
Polymorphism, Genetic
Population
Population genetics
Populations
Positive selection
Reproduction (copying)
RESEARCH ARTICLE SUMMARY
Selection, Genetic
Signatures
Whole Genome Sequencing
Title Adaptive archaic introgression of copy number variants and the discovery of previously unknown human genes
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