The Columbian Exchange as a source of adaptive introgression in human populations

AbstractAdmixture with archaic hominins has altered the landscape of genomic variation in modern human populations. Several gene regions have been previously identified as candidates of adaptive introgression (AI) that facilitated human adaptation to specific environments. However, simulation-based studies have suggested that population genetics processes other than adaptive mutations, such as heterosis from recessive deleterious variants private to populations before admixture, can also lead to patterns in genomic data that resemble adaptive introgression. The extent to which the presence of deleterious variants affect the false-positive rate and the power of current methods to detect AI has not been fully assessed. Here, we used extensive simulations to show that recessive deleterious mutations can increase the false positive rates of tests for AI compared to models without deleterious variants. We further examined candidates of AI in modern humans identified from previous studies and show that, although deleterious variants may hinder the performance of AI detection in modern humans, most signals remained robust when deleterious variants are included in the null model. While deleterious variants may have a limited impact on detecting signals of adaptive introgression in humans, we found that at least two AI candidate genes, HYAL2 and HLA, are particularly susceptible to high false positive rates due to the recessive deleterious mutations. By quantifying parameters that affect heterosis, we show that the high false positives are largely attributed to the high exon densities together with low recombination rates in the genomic regions, which can further be exaggerated by the population growth in recent human evolution. Although the combination of such parameters is rare in the human genome, caution is still warranted in other species with different genomic composition and demographic histories.

Download Full-text

The timing of human adaptation from Neanderthal introgression

10.1101/2020.10.04.325183 ◽

2020 ◽

Author(s):

Sivan Yair ◽

Kristin M. Lee ◽

Graham Coop

Keyword(s):

Demographic History ◽

Low Frequency ◽

Modern Human ◽

Allele Frequencies ◽

Population Divergence ◽

Human Populations ◽

Human Adaptation ◽

Adaptive Introgression ◽

History Of ◽

Spatio Temporal

AbstractAdmixture has the potential to facilitate adaptation by providing alleles that are immediately adaptive in a new environment or by simply increasing the long term reservoir of genetic diversity for future adaptation. A growing number of cases of adaptive introgression are being identified in species across the tree of life, however the timing of selection, and therefore the importance of the different evolutionary roles of admixture, is typically unknown. Here, we investigate the spatio-temporal history of selection favoring Neanderthal-introgressed alleles in modern human populations. Using both ancient and present-day samples of modern humans, we integrate the known demographic history of populations, namely population divergence and migration, with tests for selection. We model how a sweep placed along different branches of an admixture graph acts to modify the variance and covariance in neutral allele frequencies among populations at linked loci. Using a method based on this model of allele frequencies, we study previously identified cases of Neanderthal adaptive introgression. From these, we identify cases in which Neanderthal introgressed alleles were quickly beneficial and other cases in which they persisted at low frequency for some time. For some of the alleles that persisted at low frequency, we show that selection likely independently favored them later on in geographically separated populations. Our work highlights how admixture with ancient hominins has contributed to modern human adaptation, contextualizes observed levels of Neanderthal ancestry in present-day and ancient samples, and identifies cases of temporally varying selection that are sometimes shared across large geographic distances.

Download Full-text

Signatures of archaic adaptive introgression in present-day human populations

10.1101/045237 ◽

2016 ◽

Cited By ~ 3

Author(s):

Fernando Racimo ◽

Davide Marnetto ◽

Emilia Huerta-Sánchez

Keyword(s):

Positive Selection ◽

Candidate Genes ◽

Allele Frequency ◽

Human Populations ◽

Haplotype Structure ◽

Promising Candidate ◽

Adaptive Introgression ◽

1000 Genomes ◽

Evolutionary Advantage ◽

Mutation And Selection

AbstractComparisons of DNA from archaic and modern humans show that these groups interbred, and in some cases received an evolutionary advantage from doing so. This process - adaptive introgression - may lead to a faster rate of adaptation than is predicted from models with mutation and selection alone. Within the last couple of years, a series of studies have identified regions of the genome that are likely examples of adaptive introgression. In many cases, once a region was ascertained as being introgressed, commonly used statistics based on both haplotype as well as allele frequency information were employed to test for positive selection. Introgression by itself, however, changes both the haplotype structure and the distribution of allele frequencies, thus confounding traditional tests for detecting positive selection. Therefore, patterns generated by introgression alone may lead to false inferences of positive selection. Here we explore models involving both introgression and positive selection to investigate the behavior of various statistics under adaptive introgression. In particular, we find that the number and allelic frequencies of sites that are uniquely shared between archaic humans and specific present-day populations are particularly useful for detecting adaptive introgression. We then examine the 1000 Genomes dataset to characterize the landscape of uniquely shared archaic alleles in human populations. Finally, we identify regions that were likely subject to adaptive introgression and discuss some of the most promising candidate genes located in these regions.

Download Full-text

Signatures of Archaic Adaptive Introgression in Present-Day Human Populations

Molecular Biology and Evolution ◽

10.1093/molbev/msw216 ◽

2016 ◽

pp. msw216 ◽

Cited By ~ 24

Author(s):

Fernando Racimo ◽

Davide Marnetto ◽

Emilia Huerta-Sánchez

Keyword(s):

Human Populations ◽

Adaptive Introgression

Download Full-text

The timing of human adaptation from Neanderthal introgression

Genetics ◽

10.1093/genetics/iyab052 ◽

2021 ◽

Author(s):

Sivan Yair ◽

Kristin M Lee ◽

Graham Coop

Keyword(s):

Demographic History ◽

Low Frequency ◽

Modern Human ◽

Allele Frequencies ◽

Population Divergence ◽

Human Populations ◽

Human Adaptation ◽

Adaptive Introgression ◽

History Of ◽

Spatio Temporal

Abstract Admixture has the potential to facilitate adaptation by providing alleles that are immediately adaptive in a new environment or by simply increasing the long term reservoir of genetic diversity for future adaptation. A growing number of cases of adaptive introgression are being identified in species across the tree of life, however the timing of selection, and therefore the importance of the different evolutionary roles of admixture, is typically unknown. Here, we investigate the spatio-temporal history of selection favoring Neanderthal-introgressed alleles in modern human populations. Using both ancient and present-day samples of modern humans, we integrate the known demographic history of populations, namely population divergence and migration, with tests for selection. We model how a sweep placed along different branches of an admixture graph acts to modify the variance and covariance in neutral allele frequencies among populations at linked loci. Using a method based on this model of allele frequencies, we study previously identified cases of Neanderthal adaptive introgression. From these, we identify cases in which Neanderthal introgressed alleles were quickly beneficial and other cases in which they persisted at low frequency for some time. For some of the alleles that persisted at low frequency, we show that selection likely independently favored them later on in geographically separated populations. Our work highlights how admixture with ancient hominins has contributed to modern human adaptation and contextualizes observed levels of Neanderthal ancestry in present-day and ancient samples.

Download Full-text

The Impact of Recessive Deleterious Variation on Signals of Adaptive Introgression in Human Populations

Genetics ◽

10.1534/genetics.120.303081 ◽

2020 ◽

Vol 215 (3) ◽

pp. 799-812 ◽

Cited By ~ 3

Author(s):

Xinjun Zhang ◽

Bernard Kim ◽

Kirk E. Lohmueller ◽

Emilia Huerta-Sánchez

Keyword(s):

Human Genome ◽

False Positive ◽

False Positive Rate ◽

Genomic Variation ◽

Human Populations ◽

Deleterious Mutations ◽

Recombination Rates ◽

Adaptive Mutations ◽

Adaptive Introgression ◽

The Impact

Admixture with archaic hominins has altered the landscape of genomic variation in modern human populations. Several gene regions have been identified previously as candidates of adaptive introgression (AI) that facilitated human adaptation to specific environments. However, simulation-based studies have suggested that population genetic processes other than adaptive mutations, such as heterosis from recessive deleterious variants private to populations before admixture, can also lead to patterns in genomic data that resemble AI. The extent to which the presence of deleterious variants affect the false-positive rate and the power of current methods to detect AI has not been fully assessed. Here, we used extensive simulations under parameters relevant for human evolution to show that recessive deleterious mutations can increase the false positive rates of tests for AI compared to models without deleterious variants, especially when the recombination rates are low. We next examined candidates of AI in modern humans identified from previous studies, and show that 24 out of 26 candidate regions remain significant, even when deleterious variants are included in the null model. However, two AI candidate genes, HYAL2 and HLA, are particularly susceptible to high false positive signals of AI due to recessive deleterious mutations. These genes are located in regions of the human genome with high exon density together with low recombination rate, factors that we show increase the rate of false-positives due to recessive deleterious mutations. Although the combination of such parameters is rare in the human genome, caution is warranted in such regions, as well as in other species with more compact genomes and/or lower recombination rates. In sum, our results suggest that recessive deleterious mutations cannot account for the signals of AI in most, but not all, of the top candidates for AI in humans, suggesting they may be genuine signals of adaptation.

Download Full-text

VolcanoFinder: genomic scans for adaptive introgression

10.1101/697987 ◽

2019 ◽

Cited By ~ 6

Author(s):

Derek Setter ◽

Sylvain Mousset ◽

Xiaoheng Cheng ◽

Rasmus Nielsen ◽

Michael DeGiorgio ◽

...

Keyword(s):

Related Species ◽

Genomic Data ◽

Composite Likelihood ◽

Genomic Variation ◽

Human Populations ◽

Closely Related Species ◽

Adaptive Introgression ◽

A Genome ◽

Wide Range ◽

Donor Species

AbstractRecent research shows that introgression between closely-related species is an important source of adaptive alleles for a wide range of taxa. Typically, detection of adaptive introgression from genomic data relies on comparative analyses that require sequence data from both the recipient and the donor species. However, in many cases, the donor is unknown or the data is not currently available. Here, we introduce a genome-scan method—VolcanoFinder—to detect recent events of adaptive introgression using polymorphism data from the recipient species only.VolcanoFinder detects adaptive introgression sweeps from the pattern of excess intermediate-frequency polymorphism they produce in the flanking region of the genome, a pattern which appears as a volcano-shape in pairwise genetic diversity.Using coalescent theory, we derive analytical predictions for these patterns. Based on these results, we develop a composite-likelihood test to detect signatures of adaptive introgression relative to the genomic background. Simulation results show that VolcanoFinder has high statistical power to detect these signatures, even for older sweeps and for soft sweeps initiated by multiple migrant haplotypes. Finally, we implement VolcanoFinder to detect archaic introgression in European and sub-Saharan African human populations, and uncovered interesting candidates in both populations, such as TSHR in Europeans and TCHH-RPTN in Africans. We discuss their biological implications and provide guidelines for identifying and circumventing artifactual signals during empirical applications of VolcanoFinder.Author summaryThe process by which beneficial alleles are introduced into a species from a closely-related species is termed adaptive introgression. We present an analytically-tractable model for the effects of adaptive introgression on non-adaptive genetic variation in the genomic region surrounding the beneficial allele. The result we describe is a characteristic volcano-shaped pattern of increased variability that arises around the positively-selected site, and we introduce an open-source method VolcanoFinder to detect this signal in genomic data. Importantly, VolcanoFinder is a population-genetic likelihood-based approach, rather than a comparative-genomic approach, and can therefore probe genomic variation data from a single population for footprints of adaptive introgression, even from a priori unknown and possibly extinct donor species.

Download Full-text

Patterns of shared signatures of recent positive selection across human populations

10.1101/109371 ◽

2017 ◽

Cited By ~ 2

Author(s):

Kelsey Elizabeth Johnson ◽

Benjamin F. Voight

Keyword(s):

Positive Selection ◽

Selective Pressure ◽

Human Populations ◽

Biological Mechanisms ◽

Molecular Phenotype ◽

Fundamental Interest ◽

Adaptive Introgression ◽

Recent Positive Selection ◽

Single Positive ◽

Selection Event

ABSTRACTScans for positive selection in human populations have identified hundreds of sites across the genome with evidence of recent adaptation. These signatures often overlap across populations, but the question of how often these overlaps represent a single ancestral event remains unresolved. If a single positive selection event spread across many populations, the same sweeping haplotype should appear in each population and the selective pressure could be common across diverse populations and environments. Identifying such shared selective events would be of fundamental interest, pointing to genomic loci and human traits important in recent history across the globe. Additionally, genomic annotations that recently became available could help attach these signatures to a potential gene and molecular phenotype that may have been selected across multiple populations. We performed a scan for positive selection using the integrated haplotype score on 20 populations, and compared sweeping haplotypes using the haplotype-clustering capability of fastPHASE to create a catalog of shared and unshared overlapping selective sweeps in these populations. Using additional genomic annotations, we connect these multi-population sweep overlaps with potential biological mechanisms at several loci, including potential new sites of adaptive introgression, the glycophorin locus associated with malarial resistance, and the alcohol dehydrogenase cluster associated with alcohol dependency.

Download Full-text

Rapid, Adaptive Human Evolution Facilitated by Admixture in the Americas

10.1093/oso/9780190945961.003.0011 ◽

2021 ◽

pp. 122-138

Author(s):

Emily T. Norris ◽

Lavanya Rishishwar ◽

I. King Jordan

Keyword(s):

Human Evolution ◽

Adaptive Evolution ◽

Modern Human ◽

Human Migration ◽

Human Populations ◽

Human Immune System ◽

Isolated Populations ◽

Adaptive Introgression ◽

Physical Isolation ◽

Source Populations

Humans have migrated from their ancestral homelands in Africa to nearly every part of the world. Human migration is characterized by a recurrent process of physical isolation and genetic diversification followed by admixture, whereby previously isolated populations come together and exchange genes. Admixture results in the introgression of alleles from ancestral source populations into hybrid admixed populations, and introgression can facilitate rapid, adaptive evolution by introducing beneficial alleles at intermediate frequencies. We provide examples of adaptive introgression between archaic and modern human populations and for admixed populations in the Americas, which were formed relatively recently via admixture among African, European, and Indigenous American ancestral populations. Adaptive introgression has had an outsized effect on the human immune system. In light of the ubiquity of admixture in human evolution, we propose that adaptive introgression is a fundamentally important mechanism for driving rapid, adaptive evolution in human populations.

Download Full-text

The sense of obligation is culturally modulated

Behavioral and Brain Sciences ◽

10.1017/s0140525x19002371 ◽

2020 ◽

Vol 43 ◽

Author(s):

Andrea Bender

Keyword(s):

Cultural Studies ◽

Cross Cultural ◽

Human Populations ◽

Cultural Group ◽

Target Article ◽

Sense Of Obligation ◽

Cross Cultural Studies

Abstract Tomasello argues in the target article that, in generalizing the concrete obligations originating from interdependent collaboration to one's entire cultural group, humans become “ultra-cooperators.” But are all human populations cooperative in similar ways? Based on cross-cultural studies and my own fieldwork in Polynesia, I argue that cooperation varies along several dimensions, and that the underlying sense of obligation is culturally modulated.

Download Full-text