skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Selection against admixture and gene regulatory divergence in a long-term primate field study
Genetic admixture is central to primate evolution. We combined 50 years of field observations of immigration and group demography with genomic data from ~9 generations of hybrid baboons to investigate the consequences of admixture in the wild. Despite no obvious fitness costs to hybrids, we found signatures of selection against admixture similar to those described for archaic hominins. These patterns were concentrated near genes where ancestry is strongly associated with gene expression. Our analyses also show that introgression is partially predictable across the genome. This study demonstrates the value of integrating genomic and field data for revealing how “genomic signatures of selection” (e.g., reduced introgression in low-recombination regions) manifest in nature; moreover, it underscores the importance of other primates as living models for human evolution.  more » « less
Award ID(s):
2018897
PAR ID:
10471563
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
American Association for the Advancement of Science
Date Published:
Journal Name:
Science
Volume:
377
Issue:
6606
ISSN:
0036-8075
Page Range / eLocation ID:
635 to 641
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract The reuse of old genetic variation can promote rapid diversification in evolutionary radiations, but in most cases, the historical events underlying this divergence are not known. For example, ancient hybridization can generate new combinations of alleles that sort into descendant lineages, potentially providing the raw material to initiate divergence. In the Mimulus aurantiacus species complex, there is evidence for widespread gene flow among members of this radiation. In addition, allelic variation in the MaMyb2 gene is responsible for differences in flower color between the closely related ecotypes of subspecies puniceus, contributing to reproductive isolation by pollinators. Previous work suggested that MaMyb2 was introgressed into the red-flowered ecotype of puniceus. However, additional taxa within the radiation have independently evolved red flowers from their yellow-flowered ancestors, raising the possibility that this introgression had a more ancient origin. In this study, we used repeated tests of admixture from whole-genome sequence data across this diverse radiation to demonstrate that there has been both ancient and recurrent hybridization in this group. However, most of the signal of this ancient introgression has been removed due to selection, suggesting that widespread barriers to gene flow are in place between taxa. Yet, a roughly 30 kb region that contains the MaMyb2 gene is currently shared only among the red-flowered taxa. Patterns of admixture, sequence divergence, and extended haplotype homozygosity across this region confirm a history of ancient hybridization, where functional variants have been preserved due to positive selection in red-flowered taxa but lost in their yellow-flowered counterparts. The results of this study reveal that selection against gene flow can reduce genomic signatures of ancient hybridization, but that historical introgression can provide essential genetic variation that facilitates the repeated evolution of phenotypic traits between lineages. 
    more » « less
  2. Due to pervasive gene flow and admixture, simple bifurcating trees often do not provide an accurate representation of relationships among diverging lineages, but limited resolution in the available genomic data and the spatial distribution of samples has hindered detailed insights regarding the evolutionary and demographic history of many species and populations. In this issue ofMolecular Ecology, Foote et al. (2019) combine a powerful sampling design with novel analytical methods adopted from human genetics to describe previously unrecognized patterns of recurrent vicariance and admixture among lineages in the globally distributed killer whale (Orcinus orca). Based on sequence data from modern samples alone, they discover clear signatures of ancient admixture with a now extinct “ghost” lineage, providing one of the first accounts of archaic introgression in a nonhominid species. Coupling a cost‐effective sequencing strategy with novel analytical approaches, their paper provides a roadmap for advancing inference of evolutionary history in other nonmodel species, promising exciting times ahead for our field. 
    more » « less
  3. Large genomic insertions and deletions are a potent source of functional variation, but are challenging to resolve with short-read sequencing, limiting knowledge of the role of such structural variants (SVs) in human evolution. Here, we used a graph-based method to genotype long-read-discovered SVs in short-read data from diverse human genomes. We then applied an admixture-aware method to identify 220 SVs exhibiting extreme patterns of frequency differentiation – a signature of local adaptation. The top two variants traced to the immunoglobulin heavy chain locus, tagging a haplotype that swept to near fixation in certain southeast Asian populations, but is rare in other global populations. Further investigation revealed evidence that the haplotype traces to gene flow from Neanderthals, corroborating the role of immune-related genes as prominent targets of adaptive introgression. Our study demonstrates how recent technical advances can help resolve signatures of key evolutionary events that remained obscured within technically challenging regions of the genome. 
    more » « less
  4. ABSTRACT The application of high‐throughput sequencing to phylogenetic analyses is allowing authors to reconstruct the true evolutionary history of species. This work can illuminate specific mechanisms underlying divergence when combined with analyses of gene flow, recombination and selection. We conducted a phylogenomic analysis ofCatharus, a songbird genus with considerable potential for gene flow, variation in migratory behaviour and genomic resources. We documented discordance among trees constructed for mitochondrial, autosomal and sex (Z) chromosome partitions. Two trees were recovered on the Z. Both trees differed from the autosomes, one matched the mitochondria, and the other was unique to the Z. Gene flow with one species likely generated much of this discordance; substantial admixture betweenustulatusand the remaining species was documented and linked to at least two historic events. The tree unique to the Z likely reflects the true history ofCatharus; local genomic analyses recovered the same tree in autosomal regions with reduced admixture and recombination. Genes previously connected to migration were enriched in these regions suggesting transitions between migratory and non‐migratory states helped generate divergence. Migratory (vs. nonmigratory)Catharusformed a monophyletic clade in a subset of genomic regions. Gene flow was elevated in some of these regions suggesting adaptive introgression may have occurred, but the dominant pattern was of balancing selection maintaining ancestral polymorphisms important for olfaction and perhaps, by extension, adaptation to temperate climates. This work illuminates the evolutionary history of an important model in speciation and demonstrates how differential resistance to gene flow can affect local genomic patterns. 
    more » « less
  5. Parsch, John (Ed.)
    Abstract Genetic introgression not only provides material for adaptive evolution but also confounds our understanding of evolutionary history. This is particularly true for canids, a species complex in which genome sequencing and analysis has revealed a complex history of admixture and introgression. Here, we sequence 19 new whole genomes from high-altitude Tibetan and Himalayan wolves and dogs and combine these into a larger data set of 166 whole canid genomes. Using these data, we explore the evolutionary history and adaptation of these and other canid lineages. We find that Tibetan and Himalayan wolves are closely related to each other, and that ∼39% of their nuclear genome is derived from an as-yet-unrecognized wolf-like lineage that is deeply diverged from living Holarctic wolves and dogs. The EPAS1 haplotype, which is present at high frequencies in Tibetan dog breeds and wolves and confers an adaptive advantage to animals living at high altitudes, was probably derived from this ancient lineage. Our study underscores the complexity of canid evolution and demonstrates how admixture and introgression can shape the evolutionary trajectories of species. 
    more » « less