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Hahn, M. W.

Publications and source records attributed to Hahn, M. W..

60 records · Page 4Linked to original sources

Dissecting the basis of novel trait evolution in a radiation with widespread phylogenetic discordance

Phylogenetic analyses of trait evolution can provide insight into the evolutionary processes that initiate and drive phenotypic diversification. However, recent phylogenomic studies have revealed extensive gene tree-species tree discordance, which can lead to incorrect inferences of trait evolution if only a single species tree is used for analysis. This phenomenon--dubbed \"hemiplasy\"--is particularly important to consider during analyses of character evolution in rapidly radiating groups, where discordance is widespread. Here we generate whole-transcriptome data for a phylogenetic analysis of 14 species in the plant genus Jaltomata (the sister clade to Solanum), which has experienced rapid, recent trait evolution, including in fruit and nectar color, and flower size and shape. Consistent with other radiations, we find evidence for rampant gene tree discordance due to incomplete lineage sorting (ILS) and several introgression events among the well-supported subclades. Since both ILS and introgression increase the probability of hemiplasy, we perform several analyses that take discordance into account while identifying genes that might contribute to phenotypic evolution. Despite discordance, the history of fruit color evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit color variation. In contrast, hemiplasy appears to strongly affect inferences about floral character transitions in Jaltomata, and we identify candidate loci that could arise either from multiple lineage-specific substitutions or standing ancestral polymorphisms. Our analysis provides a generalizable example of how to manage discordance when identifying loci associated with trait evolution in a radiating lineage.

evolutionary biology↗

Multinucleotide mutations cause false inferences of positive selection

Phylogenetic tests of adaptive evolution, which infer positive selection from an excess of nonsynonymous changes, assume that nucleotide substitutions occur singly and independently. But recent research has shown that multiple errors at adjacent sites often occur in single events during DNA replication. These multinucleotide mutations (MNMs) are overwhelmingly likely to be nonsynonymous. We therefore evaluated whether phylogenetic tests of adaptive evolution, such as the widely used branch-site test, might misinterpret sequence patterns produced by MNMs as false support for positive selection. We explored two genome-wide datasets comprising thousands of coding alignments - one from mammals and one from flies - and found that codons with multiple differences (CMDs) account for virtually all the support for lineage-specific positive selection inferred by the branch-site test. Simulations under genome-wide, empirically derived conditions without positive selection show that realistic rates of MNMs cause a strong and systematic bias in the branch-site and related tests; the bias is sufficient to produce false positive inferences approximately as often as the branch-site test infers positive selection from the empirical data. Our analysis indicates that genes may often be inferred to be under positive selection simply because they stochastically accumulated one or a few MNMs. Because these tests do not reliably distinguish sequence patterns produced by authentic positive selection from those caused by neutral fixation of MNMs, many published inferences of adaptive evolution using these techniques may therefore be artifacts of model violation caused by unincorporated neutral mutational processes. We develop an alternative model that incorporates MNMs and may be helpful in reducing this bias.

evolutionary biology↗

Speciation as a sieve for ancestral polymorphism

Studying the process of speciation using patterns of genomic divergence between species requires that we understand the determinants of genetic diversity within species. Because sequence diversity in an ancestral population determines the starting point from which divergent populations accumulate differences (Gillespie & Langley 1979), any evolutionary forces that shape diversity within species can have a large impact on measures of divergence between species. These forces include those both decreasing (e.g., selective sweeps (Begun et al. 2007; Cruickshank & Hahn 2014) or background selection (Phung et al. 2016)) and increasing variation (e.g., balancing selection (Charlesworth 2006)). Selection can increase diversity by favoring the maintenance of polymorphism via overdominance, frequency dependence, and heterogeneous selection. Nevertheless, balanced polymorphisms are co ...

evolutionary biology↗

Why concatenation fails in the anomaly zone

AbstrctGenome-scale sequencing has been of great benefit in recovering species trees, but has not provided final answers. Despite the rapid accumulation of molecular sequences, resolving short and deep branches of the tree of life has remained a challenge, and has prompted the development of new strategies that can make the best use of available data. One such strategy - the concatenation of gene alignments - can be successful when coupled with many tree estimation methods, but has also been shown to fail when there are high levels of incomplete lineage sorting. Here, we focus on the failure of likelihood-based methods in retrieving a rooted, asymmetric four-taxon species tree from concatenated data when the species tree is in or near the anomaly zone - a region of parameter space where the most common gene tree does not match the species tree because of incomplete lineage sorting. First, we use coalescent theory to prove that most informative sites will support the species tree in the anomaly zone, and that as a consequence maximum-parsimony succeeds in recovering the species tree from concatenated data. We further show that maximum-likelihood tree estimation from concatenated data fails both inside and outside the anomaly zone, and that this failure is unconnected to the frequency of the most common gene tree. We provide support for a hypothesis that likelihood-based methods fail in and near the anomaly zone because discordant sites on the species tree have a lower likelihood than those that are discordant on alternative topologies. Our results confirm and extend previous reports of the failure and success of likelihood- and parsimony-based methods, and highlight avenues for future work improving the performance of methods aimed at recovering species tree.

evolutionary biology↗

The effects of increasing the number of taxa on inferences of molecular convergence

Convergent evolution provides insight into the link between phenotype and genotype. Recently, large-scale comparative studies of convergent evolution have become possible, but researchers are still trying to determine the best way to design these types of analyses. One aspect of molecular convergence studies that has not yet been investigated is how taxonomic sample size affects inferences of molecular convergence. Here we show that increased sample size decreases the amount of inferred molecular convergence associated with the three convergent transitions to a marine environment in mammals. The sampling of more taxa--both with and without the convergent phenotype--reveals that alleles associated only with marine mammals in small datasets are actually more widespread, or are not shared by all marine species. The sampling of more taxa also allows finer resolution of ancestral substitutions, revealing that they are not in fact on lineages leading to solely marine species. We revisit a previous study on marine mammals and find that only 7 of the reported 43 genes with convergent substitutions still show signs of convergence with a larger number of background species. However, 4 of those 7 genes also showed signs of positive selection in the original analysis and may still be good candidates for adaptive convergence. Though our study is framed around the convergence of marine mammals, we expect our conclusions on taxonomic sampling are generalizable to any study of molecular convergence.

genomics↗

Linking gene expression to unilateral pollen-pistil reproductive barriers

Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. UI is characterized by a compatible interaction between partners in one direction, but in the reciprocal cross fertilization fails, generally due to pollen tube rejection by the pistil. Although UI has long been observed in crosses between different species, the underlying molecular mechanisms are only beginning to be characterized. The wild tomato relative Solanum habrochaites provides a unique study system to investigate the molecular basis of this reproductive barrier, as populations within the species exhibit both interspecific and interpopulation UI. Here we used a transcriptomic approach to identify genes in both pollen and pistil tissues that may be probable key players in UI. We confirmed UI at the pollen-pistil level between a self-incompatible population and a self-compatible population of S. habrochaites. A comparison of gene expression between pollinated styles exhibiting the incompatibility response and unpollinated controls revealed only a small number of differentially expressed transcripts. Many more differences in transcript profiles were identified between UI-competent versus UI-compromised reproductive tissues. A number of intriguing candidate genes were highly differentially expressed, including a putative pollen arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone Rapid Alkalinization Factor. Our data also provide transcriptomic evidence that fundamental processes including reactive oxygen species signaling are likely key in UI pollen-pistil interactions between both populations and species. Our transcriptomic analysis highlighted specific genes, including those in ROS signaling pathways that warrant further study in investigations of UI. To our knowledge, this is the first report to identify candidate genes involved in unilateral barriers between populations of the same species.

plant biology↗