The genomic consequences of hybridization

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Abstract

In the past decade, advances in genome sequencing have allowed researchers to uncover the history of hybridization in diverse groups of species, including our own. Although the field has made impressive progress in documenting the extent of natural hybridization, both historical and recent, there are still many unanswered questions about its genetic and evolutionary consequences. Recent work has suggested that the outcomes of hybridization in the genome may be in part predictable, but many open questions about the nature of selection on hybrids and the biological variables that shape such selection have hampered progress in this area. We synthesize what is known about the mechanisms that drive changes in ancestry in the genome after hybridization, highlight major unresolved questions, and discuss their implications for the predictability of genome evolution after hybridization.

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Most cited references 289

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The genomic basis of adaptive evolution in threespine sticklebacks

Felicity Jones, Manfred Grabherr, Yingguang Frank Chan … (2012)

Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.

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Chromosome inversions, local adaptation and speciation.

Mark Kirkpatrick, Nick Barton (2006)

We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.

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The landscape of Neandertal ancestry in present-day humans

Sriram Sankararaman, Swapan Mallick, Michael Dannemann … (2014)

Analyses of Neandertal genomes have revealed that Neandertals have contributed genetic variants to modern humans 1–2 . The antiquity of Neandertal gene flow into modern humans means that regions that derive from Neandertals in any one human today are usually less than a hundred kilobases in size. However, Neandertal haplotypes are also distinctive enough that several studies have been able to detect Neandertal ancestry at specific loci 1,3–8 . Here, we have systematically inferred Neandertal haplotypes in the genomes of 1,004 present-day humans 12 . Regions that harbor a high frequency of Neandertal alleles in modern humans are enriched for genes affecting keratin filaments suggesting that Neandertal alleles may have helped modern humans adapt to non-African environments. Neandertal alleles also continue to shape human biology, as we identify multiple Neandertal-derived alleles that confer risk for disease. We also identify regions of millions of base pairs that are nearly devoid of Neandertal ancestry and enriched in genes, implying selection to remove genetic material derived from Neandertals. Neandertal ancestry is significantly reduced in genes specifically expressed in testis, and there is an approximately 5-fold reduction of Neandertal ancestry on chromosome X, which is known to harbor a disproportionate fraction of male hybrid sterility genes 20–22 . These results suggest that part of the reduction in Neandertal ancestry near genes is due to Neandertal alleles that reduced fertility in males when moved to a modern human genetic background.

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Author and article information

Contributors

Benjamin M Moran:

ORCID: https://orcid.org/0000-0001-5230-0863

Cheyenne Payne:

ORCID: https://orcid.org/0000-0003-4651-3824

Molly Schumer:

ORCID: https://orcid.org/0000-0002-2075-5668

Patricia J Wittkopp: Role: Reviewing Editor

Patricia J Wittkopp: Role: Senior Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 04 August 2021

Publication date Collection: 2021

Volume: 10

Electronic Location Identifier: e69016

Affiliations

[1 ] Department of Biology, Stanford University Stanford United States

[2 ] Centro de Investigaciones Científicas de las Huastecas “Aguazarca” Hidalgo Mexico

[3 ] Department of Ecology, Evolution & Behavior and Plant and Microbial Biology, University of Minnesota Minneapolis United States

[4 ] Hanna H. Gray Fellow, Howard Hughes Medical Institute Stanford United States

University of Michigan United States

Author notes

[†]

These authors contributed equally to this work.

Author information

Benjamin M Moran https://orcid.org/0000-0001-5230-0863

Cheyenne Payne https://orcid.org/0000-0003-4651-3824

Daniel L Powell https://orcid.org/0000-0001-9204-645X

Molly Schumer https://orcid.org/0000-0002-2075-5668

Article

Publisher ID: 69016

DOI: 10.7554/eLife.69016

PMC ID: 8337078

PubMed ID: 34346866

SO-VID: c8e9c0ef-a9c8-4a66-adbe-0f4b89432363

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 01 April 2021

Date accepted : 09 July 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 2019273798

Award Recipient : Benjamin M Moran

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 2010950

Award Recipient : Quinn Langdon

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 1753632

Award Recipient : Yaniv Brandvain

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: 1754246

Award Recipient : Yaniv Brandvain

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: 1R35GM133774

Award Recipient : Molly Schumer

Funded by: FundRef http://dx.doi.org/10.13039/100011099, Center for Computational, Evolutionary and Human Genomics, Stanford University;

Award Recipient : Quinn Langdon

Funded by: FundRef http://dx.doi.org/10.13039/100005492, Stanford University;

Award ID: Knight-Hennessy Scholars Fellowship

Award Recipient : Benjamin M Moran

Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;

Award ID: Hanna H. Gray Fellow

Award Recipient : Molly Schumer

Funded by: FundRef http://dx.doi.org/10.13039/100004412, Human Frontier Science Program;

Award ID: Human Frontiers in Science Young Investigator Award

Award Recipient : Molly Schumer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement A synthesis of recent hybridization literature reveals emerging patterns in the evolution of genomes after hybridization, processes proposed to explain those patterns, and important open questions to direct future hybrid genomics research.

ScienceOpen disciplines: Life sciences

Keywords: hybridization,incompatibility,selection,introgression,ancestry,admixture

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: hybridization, incompatibility, selection, introgression, ancestry, admixture

The genomic consequences of hybridization

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Abstract

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Paleontology of Mongolia

Most cited references 289

The genomic basis of adaptive evolution in threespine sticklebacks

Chromosome inversions, local adaptation and speciation.

The landscape of Neandertal ancestry in present-day humans

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