Inference of Gorilla demographic and selective history from whole genome sequence data
Kimberly F. McManus, Joanna L. Kelley, Shiya Song, Krishna Veeramah, August E. Woerner, Laurie S. Stevison, Oliver A. Ryder, , Jeffrey M. Kidd, Jeffrey D. Wall, Carlos D. Bustamante, Michael F. Hammer
While population-level genomic sequence data have been gathered extensively for humans, similar data from our closest living relatives are just beginning to emerge. Examination of genomic variation within great apes offers many opportunities to increase our understanding of the forces that have differentially shaped the evolutionary history of hominid taxa. Here, we expand upon the work of the Great Ape Genome Project by analyzing medium to high coverage whole genome sequences from 14 western lowland gorillas (Gorilla gorilla gorilla), 2 eastern lowland gorillas (G. beringei graueri), and a single Cross River individual (G. gorilla diehli). We infer that the ancestors of western and eastern lowland gorillas diverged from a common ancestor ~261 thousand years ago (kya), and that the ancestors of the Cross River population diverged from the western lowland gorilla lineage ~68 kya. Using a diffusion approximation approach to model the genome-wide site frequency spectrum, we infer a history of western lowland gorillas that includes an ancestral population expansion of ~1.4-fold around ~970 kya and a recent ~5.6-fold contraction in population size ~23 kya. The latter may correspond to a major reduction in African equatorial forests around the Last Glacial Maximum. We also analyze patterns of variation among western lowland gorillas to identify several genomic regions with strong signatures of recent selective sweeps. We find that processes related to taste, pancreatic and saliva secretion, sodium ion transmembrane transport, and cardiac muscle function are overrepresented in genomic regions predicted to have experienced recent positive selection.
Non-crossover gene conversions show strong GC bias and unexpected clustering in humans
Amy Williams, Giulio Geneovese, Thomas Dyer, Katherine Truax, Goo Jun, Nick Patterson, Joanne E. Curran, Ravi Duggirala, John Blangero, David Reich, Molly Przeworski,
Although the past decade has seen tremendous progress in our understanding of fine-scale recombination, little is known about non-crossover (or “gene conversion”) resolutions. We report the first genome-wide study of non-crossover gene conversion events in humans. Using SNP array data from 94 meioses, we identified 107 sites affected by non-crossover events, of which 51/53 were confirmed in sequence data. Our results suggest that a site is involved in a non-crossover event at a rate of 6.7 × 10-6/bp/generation, consistent with results from sperm-typing studies. Observed non-crossover events show strong allelic bias, with 70% (61–79%) of events transmitting GC alleles (P=7.9 × 10-5), and have tracts lengths that vary over more than an order of magnitude. Strikingly, in 4 of 15 regions with available resequencing data, multiple (~2–4) distinct non-crossover events cluster within ~20–30 kb. This pattern has not been reported previously in mammals and is inconsistent with canonical models of double strand break repair.
Characterization of the transcriptome, nucleotide sequence polymorphism, and natural selection in the desert adapted mouse Peromyscus eremicus
Matthew D MacManes, Michael B Eisen
As a direct result of intense heat and aridity, deserts are thought to be among the most harsh of environments, particularly for their mammalian inhabitants. Given that osmoregulation can be challenging for these animals, with failure resulting in death, strong selection should be observed on genes related to the maintenance of water and solute balance. One such animal, Peromyscus eremicus, is native to the desert regions of the southwest United States and may live its entire life without oral fluid intake. As a first step toward understanding the genetics that underlie this phenotype, we present a characterization of the P. eremicus transcriptome. We assay four tissues (kidney, liver, brain, testes) from a single individual and supplement this with population level renal transcriptome sequencing from 15 additional animals. We identified a set of transcripts undergoing both purifying and balancing selection based on estimates of Tajima’s D. In addition, we used the branch-site test to identify a transcript – Slc2a9, likely related to desert osmoregulation – undergoing enhanced selection in P. eremicus relative to a set of related non-desert rodents.
Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the southeastern United States and Caribbean Islands
Joyce Y Kao, Asif Zubair, Matthew P Salomon, Sergey V Nuzhdin, Daniel Campo
Genome sequences from North American Drosophila melanogaster populations have become available to the scientific community. Deciphering the underlying population structure of these resources is crucial to make the most of these population genomic resources. Accepted models of North American colonization generally purport that several hundred years ago, flies from Africa and Europe were transported to the east coast United States and the Caribbean Islands respectively and thus current east coast US and Caribbean populations are an admixture of African and European ancestry. Theses models have been constructed based on phenotypes and limited genetic data. In our study, we have sequenced individual whole genomes of flies from populations in the southeast US and Caribbean Islands and examined these populations in conjunction with population sequences from Winters, CA, (USA); Raleigh, NC (USA); Cameroon (Africa); and Montpellier (France) to uncover the underlying population structure of North American populations. We find that west coast US populations are most like European populations likely reflecting a rapid westward expansion upon first settlements into North America. We also find genomic evidence of African and European admixture in east coast US and Caribbean populations, with a clinal pattern of decreasing proportions of African ancestry with higher latitude further supporting the proposed demographic model of Caribbean flies being established by African ancestors. Our genomic analysis of Caribbean flies is the first study that exposes the source of previously reported novel African alleles found in east coast US populations.
Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster
Alan O. Bergland, Ray Tobler, Josefa Gonzalez, Paul Schmidt, Dmitri Petrov
Populations arrayed along broad latitudinal gradients often show patterns of clinal variation in phenotype and genotype. Such population differentiation can be generated and maintained by a combination of demographic events and adaptive evolutionary processes. Here, we investigate the evolutionary forces that generated and maintain clinal variation genome-wide among populations of Drosophila melanogaster sampled in North America and Australia. We contrast patterns of clinal variation in these continents with patterns of differentiation among ancestral European and African populations. We show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this admixture event generated genome-wide patterns of parallel clinal variation. The pervasive effects of admixture meant that only a handful of loci could be attributed to the operation of spatially varying selection using an FST outlier approach. Our results provide novel insight into a well-studied system of clinal differentiation and provide a context for future studies seeking to identify loci contributing to local adaptation in D. melanogaster.
Estimating the temporal and spatial extent of gene flow among sympatric lizard populations (genus Sceloporus) in the southern Mexican highlands
Jared A Grummer, Martha L. Calderón, Adrián Nieto Montes-de Oca, Eric N Smith, Fausto Mendez-de la Cruz, Adam Leache
Interspecific gene flow is pervasive throughout the tree of life. Although detecting gene flow between populations has been facilitated by new analytical approaches, determining the timing and geography of hybridization has remained difficult, particularly for historical gene flow. A geographically explicit phylogenetic approach is needed to determine the ancestral population overlap. In this study, we performed population genetic analyses, species delimitation, simulations, and a recently developed approach of species tree diffusion to infer the phylogeographic history, timing and geographic extent of gene flow in the Sceloporus spinosus group. The two species in this group, S. spinosus and S. horridus, are distributed in eastern and western portions of Mexico, respectively, but populations of these species are sympatric in the southern Mexican highlands. We generated data consisting of three mitochondrial genes and eight nuclear loci for 148 and 68 individuals, respectively. We delimited six lineages in this group, but found strong evidence of mito-nuclear discordance in sympatric populations of S. spinosus and S. horridus owing to mitochondrial introgression. We used coalescent simulations to differentiate ancestral gene flow from secondary contact, but found mixed support for these two models. Bayesian phylogeography indicated more than 60% range overlap between ancestral S. spinosus and S. horridus populations since the time of their divergence. Isolation-migration analyses, however, revealed near-zero levels of gene flow between these ancestral populations. Interpreting results from both simulations and empirical data indicate that despite a long history of sympatry among these two species, gene flow in this group has only recently occurred.
Rate and cost of adaptation in the Drosophila genome
Stephan Schiffels, Michael Lässig, Ville Mustonen
Recent studies have consistently inferred high rates of adaptive molecular evolution between Drosophila species. At the same time, the Drosophila genome evolves under different rates of recombination, which results in partial genetic linkage between alleles at neighboring genomic loci. Here we analyze how linkage correlations affect adaptive evolution. We develop a new inference method for adaptation that takes into account the effect on an allele at a focal site caused by neighboring deleterious alleles (background selection) and by neighboring adaptive substitutions (hitchhiking). Using complete genome sequence data and fine-scale recombination maps, we infer a highly heterogeneous scenario of adaptation in Drosophila. In high-recombining regions, about 50% of all amino acid substitutions are adaptive, together with about 20% of all substitutions in proximal intergenic regions. In low-recombining regions, only a small fraction of the amino acid substitutions are adaptive, while hitchhiking accounts for the majority of these changes. Hitchhiking of deleterious alleles generates a substantial collateral cost of adaptation, leading to a fitness decline of about 30/2N per gene and per million years in the lowest-recombining regions. Our results show how recombination shapes rate and efficacy of the adaptive dynamics in eukaryotic genomes.