Abstract
Phylogenomics has revealed the remarkable frequency with which introgression occurs across the tree of life. These discoveries have been enabled by the rapid growth of methods designed to ...detect and characterize introgression from whole-genome sequencing data. A large class of phylogenomic methods makes use of data across species to infer and characterize introgression based on expectations from the multispecies coalescent. These methods range from simple tests, such as the D-statistic, to model-based approaches for inferring phylogenetic networks. Here, we provide a detailed overview of the various signals that different modes of introgression are expected leave in the genome, and how current methods are designed to detect them. We discuss the strengths and pitfalls of these approaches and identify areas for future development, highlighting the different signals of introgression, and the power of each method to detect them. We conclude with a discussion of current challenges in inferring introgression and how they could potentially be addressed.
It is now understood that introgression can serve as powerful evolutionary force, providing genetic variation that can shape the course of trait evolution. Introgression also induces a shared ...evolutionary history that is not captured by the species phylogeny, potentially complicating evolutionary analyses that use a species tree. Such analyses are often carried out on gene expression data across species, where the measurement of thousands of trait values allows for powerful inferences while controlling for shared phylogeny. Here, we present a Brownian motion model for quantitative trait evolution under the multispecies network coalescent framework, demonstrating that introgression can generate apparently convergent patterns of evolution when averaged across thousands of quantitative traits. We test our theoretical predictions using whole-transcriptome expression data from ovules in the wild tomato genus Solanum. Examining two sub-clades that both have evidence for post-speciation introgression, but that differ substantially in its magnitude, we find patterns of evolution that are consistent with histories of introgression in both the sign and magnitude of ovule gene expression. Additionally, in the sub-clade with a higher rate of introgression, we observe a correlation between local gene tree topology and expression similarity, implicating a role for introgressed cis-regulatory variation in generating these broad-scale patterns. Our results reveal a general role for introgression in shaping patterns of variation across many thousands of quantitative traits, and provide a framework for testing for these effects using simple model-informed predictions.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to ...increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
A Three-Sample Test for Introgression Hahn, Matthew W; Hibbins, Mark S
Molecular biology and evolution,
12/2019, Volume:
36, Issue:
12
Journal Article
Peer reviewed
Open access
Abstract
Many methods exist for detecting introgression between nonsister species, but the most commonly used require either a single sequence from four or more taxa or multiple sequences from each ...of three taxa. Here, we present a test for introgression that uses only a single sequence from three taxa. This test, denoted D3, uses similar logic as the standard D-test for introgression, but by using pairwise distances instead of site patterns it is able to detect the same signal of introgression with fewer species. We use simulations to show that D3 has statistical power almost equal to D, demonstrating its use on a data set of wild bananas (Musa). The new test is easy to apply and easy to interpret, and should find wide use among currently available data sets.
Introgression is a pervasive biological process, and many statistical methods have been developed to infer its presence from genomic data. However, many of the consequences and genomic signatures of ...introgression remain unexplored from a methodological standpoint. Here, we develop a model for the timing and direction of introgression based on the multispecies network coalescent, and from it suggest new approaches for testing introgression hypotheses. We suggest two new statistics,
and
, which can be used in conjunction with other information to test hypotheses relating to the timing and direction of introgression, respectively.
may find use in evaluating cases of homoploid hybrid speciation (HHS), while
provides a four-taxon test for polarizing introgression. Although analytical expectations for our statistics require a number of assumptions to be met, we show how simulations can be used to test hypotheses about introgression when these assumptions are violated. We apply the
statistic to genomic data from the wild yeast
-a proposed example of HHS-demonstrating its use as a test of this model. These methods provide new and powerful ways to address questions relating to the timing and direction of introgression.
Phylogenetic comparative methods have long been a mainstay of evolutionary biology, allowing for the study of trait evolution across species while accounting for their common ancestry. These analyses ...typically assume a single, bifurcating phylogenetic tree describing the shared history among species. However, modern phylogenomic analyses have shown that genomes are often composed of mosaic histories that can disagree both with the species tree and with each other-so-called discordant gene trees. These gene trees describe shared histories that are not captured by the species tree, and therefore that are unaccounted for in classic comparative approaches. The application of standard comparative methods to species histories containing discordance leads to incorrect inferences about the timing, direction, and rate of evolution. Here, we develop two approaches for incorporating gene tree histories into comparative methods: one that constructs an updated phylogenetic variance-covariance matrix from gene trees, and another that applies Felsenstein's pruning algorithm over a set of gene trees to calculate trait histories and likelihoods. Using simulation, we demonstrate that our approaches generate much more accurate estimates of tree-wide rates of trait evolution than standard methods. We apply our methods to two clades of the wild tomato genus
with varying rates of discordance, demonstrating the contribution of gene tree discordance to variation in a set of floral traits. Our approaches have the potential to be applied to a broad range of classic inference problems in phylogenetics, including ancestral state reconstruction and the inference of lineage-specific rate shifts.
The incongruence of character states with phylogenetic relationships is often interpreted as evidence of convergent evolution. However, trait evolution along discordant gene trees can also generate ...these incongruences - a phenomenon known as hemiplasy. Classic comparative methods do not account for discordance, resulting in incorrect inferences about the number, timing, and direction of trait transitions. Biological sources of discordance include incomplete lineage sorting (ILS) and introgression, but only ILS has received theoretical consideration in the context of hemiplasy. Here, we present a model that shows introgression makes hemiplasy more likely, such that methods that account for ILS alone will be conservative. We also present a method and software (
) for making statistical inferences about the probability of hemiplasy and homoplasy in large datasets that contain both ILS and introgression. We apply our methods to two empirical datasets, finding that hemiplasy is likely to contribute to the observed trait incongruences in both.
An increasing number of phylogenomic studies have documented a clear “footprint” of postspeciation introgression among closely related species. Nonetheless, systematic genome‐wide studies of factors ...that determine the likelihood of introgression remain rare. Here, we propose an a priori hypothesis‐testing framework that uses introgression statistics—including a new metric of estimated introgression, Dp—to evaluate general patterns of introgression prevalence and direction across multiple closely related species. We demonstrate this approach using whole genome sequences from 32 lineages in 11 wild tomato species to assess the effect of three factors on introgression—genetic relatedness, geographical proximity, and mating system differences—based on multiple trios within the “ABBA–BABA” test. Our analyses suggest each factor affects the prevalence of introgression, although our power to detect these is limited by the number of comparisons currently available. We find that of 14 species pairs with geographically “proximate” versus “distant” population comparisons, 13 showed evidence of introgression; in 10 of these cases, this was more prevalent between geographically closer populations. We also find modest evidence that introgression declines with increasing genetic divergence between lineages, is more prevalent between lineages that share the same mating system, and—when it does occur between mating systems—tends to involve gene flow from more inbreeding to more outbreeding lineages. Although our analysis indicates that recent postspeciation introgression is frequent in this group—detected in 15 of 17 tested trios—estimated levels of genetic exchange are modest (0.2–2.5% of the genome), so the relative importance of hybridization in shaping the evolutionary trajectories of these species could be limited. Regardless, similar clade‐wide analyses of genomic introgression would be valuable for disentangling the major ecological, reproductive, and historical determinants of postspeciation gene flow, and for assessing the relative contribution of introgression as a source of genetic variation.
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FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Edible bananas result from interspecific hybridization between Musa acuminata and Musa balbisiana, as well as among subspecies in M. acuminata. Four particular M. acuminata subspecies have been ...proposed as the main contributors of edible bananas, all of which radiated in a short period of time in southeastern Asia. Clarifying the evolution of these lineages at a whole-genome scale is therefore an important step toward understanding the domestication and diversification of this crop. This study reports the de novo genome assembly and gene annotation of a representative genotype from three different subspecies of M. acuminata. These data are combined with the previously published genome of the fourth subspecies to investigate phylogenetic relationships. Analyses of shared and unique gene families reveal that the four subspecies are quite homogenous, with a core genome representing at least 50% of all genes and very few M. acuminata species-specific gene families. Multiple alignments indicate high sequence identity between homologous single copy-genes, supporting the close relationships of these lineages. Interestingly, phylogenomic analyses demonstrate high levels of gene tree discordance, due to both incomplete lineage sorting and introgression. This pattern suggests rapid radiation within Musa acuminata subspecies that occurred after the divergence with M. balbisiana. Introgression between M. a. ssp. malaccensis and M. a. ssp. burmannica was detected across the genome, though multiple approaches to resolve the subspecies tree converged on the same topology. To support evolutionary and functional analyses, we introduce the PanMusa database, which enables researchers to exploration of individual gene families and trees.
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