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bioRxiv2014

Generation of a Panel of Induced Pluripotent Stem Cells From Chimpanzees: a Resource for Comparative Functional Genomics

Comparative genomics studies in primates are extremely restricted because we only have access to a few types of cell lines from non-human apes and to a limited collection of frozen tissues. In order to gain better insight into regulatory processes that underlie variation in complex phenotypes, we must have access to faithful model systems for a wide range of tissues and cell types. To facilitate this, we have generated a panel of 7 fully characterized chimpanzee (Pan troglodytes) induced pluripotent stem cell (iPSC) lines derived from fibroblasts of healthy donors. All lines appear to be free of integration from exogenous reprogramming vectors, can be maintained using standard iPSC culture techniques, and have proliferative and differentiation potential similar to human and mouse lines. To begin demonstrating the utility of comparative iPSC panels, we collected RNA sequencing data and methylation profiles from the chimpanzee iPSCs and their corresponding fibroblast precursors, as well as from 7 human iPSCs and their precursors, which were of multiple cell type and population origins. Overall, we observed much less regulatory variation within species in the iPSCs than in the somatic precursors, indicating that the reprogramming process has erased many of the differences observed between somatic cells of different origins. We identified 4,918 differentially expressed genes and 3,598 differentially methylated regions between iPSCs of the two species, many of which are novel inter-species differences that were not observed between the somatic cells of the two species. Our panel will help realise the potential of iPSCs in primate studies, and in combination with genomic technologies, transform studies of comparative evolution.

Evolutionary Biology↗

bioRxiv2014

Evolving mutation rate advances invasion speed of sexual species

Many species are shifting their ranges in response to global climate change. The evolution of dispersal during range expansion increases invasion speed, provided that a species can adapt sufficiently fast to novel local conditions. Mutation rates can evolve too, under conditions that favor an increased rate of adaptation. However, evolution at the mutator gene has thus far been deemed of minor importance in sexual populations due to its dependence on genetic hitchhiking with a beneficial mutation at a gene under selection, and thus its sensitivity to recombination. Here we use an individual-based model to show that the mutator gene and the gene under selection can be effectively linked at the population level during invasion. This causes the evolutionary increase of mutation rates in sexual populations, even if they are not linked at the individual level. The observed evolution of mutation rate is adaptive and clearly advances range expansion both through its effect on the evolution of dispersal rate, and the evolution of local adaptation. In addition, we observe the evolution of mutation rates in a spatially stable population under strong directional selection, but not when we add variance to the mean selection pressure. By this we extend the existing theory on the evolution of mutation rates, which is generally thought to be limited to asexual populations, with possibly far-reaching consequences concerning invasiveness and the rate at which species can adapt to novel environmental conditions as experienced under global climate change.

Evolutionary Biology↗

bioRxiv2014

Secondary contact and local adaptation contribute to genome-wide patterns of clinal variation in Drosophila melanogaster

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 historical demographic events and local adaptation. These evolutionary forces are not mutually exclusive and, moreover, can in some cases produce nearly identical patterns of genetic differentiation among populations. 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. Using established and novel methods we derive here, we show that recently derived North America and Australia populations were likely founded by both European and African lineages and that this admixture event contributed to 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 the well-studied system of clinal differentiation in D. melanogaster and provide a context for future studies seeking to identify loci contributing to local adaptation in a wide variety of organisms, including other invasive species as well as some temperate endemics.

Evolutionary Biology↗

bioRxiv2014

Population genomic analysis uncovers African and European admixture in Drosophila melanogaster populations from the southeastern United States and Caribbean Islands

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.

Evolutionary Biology↗

bioRxiv2014

Self-fertilization and inbreeding limit the scope for sexual antagonism

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here we explore how self-fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, since inbreeding reduces the frequency of heterozygotes and speeds fixation. Although this expectation was supported, our results show that there is an interactive effect between the degree of selfing and dominance such that those segregating sexually antagonistic loci that do exist are more likely to be partially dominant. In addition, inbreeding effects may influence population persistence and genomic location of sexually antagonistic loci in separate-sexed organisms.

Evolutionary Biology↗

bioRxiv2014

Genome-Wide Mapping In A House Mouse Hybrid Zone Reveals Hybrid Sterility Loci And Dobzhansky-Muller Interactions

Mapping hybrid defects in contact zones between incipient species can identify genomic regions contributing to reproductive isolation and reveal genetic mechanisms of speciation. The house mouse features a rare combination of sophisticated genetic tools and natural hybrid zones between subspecies. Male hybrids often show reduced fertility, a common reproductive barrier between incipient species. Laboratory crosses have identified sterility loci, but each encompasses hundreds of genes. We map genetic determinants of testis weight and testis gene expression using offspring of mice captured in a hybrid zone between M. musculus musculus and M. m. domesticus. Many generations of admixture enables high-resolution mapping of loci contributing to these sterility-related phenotypes. We identify complex interactions among sterility loci, suggesting multiple, non-independent genetic incompatibilities contribute to barriers to gene flow in the hybrid zone.

Evolutionary Biology↗

bioRxiv2014

On the prospect of identifying adaptive loci in recently bottlenecked populations

Identifying adaptively important loci in recently bottlenecked populations - be it natural selection acting on a population following the colonization of novel habitats in the wild, or artificial selection during the domestication of a breed - remains a major challenge. Here we report the results of a simulation study examining the performance of available population-genetic tools for identifying genomic regions under selection. To illustrate our findings, we examined the interplay between selection and demography in two species of Peromyscus mice, for which we have independent evidence of selection acting on phenotype as well as functional evidence identifying the underlying genotype. With this unusual information, we tested whether population-genetic-based approaches could have been utilized to identify the adaptive locus. Contrary to published claims, we conclude that the use of the background site frequency spectrum as a null model is largely ineffective in bottlenecked populations. Results are quantified both for site frequency spectrum and linkage disequilibrium-based predictions, and are found to hold true across a large parameter space that encompasses many species and populations currently under study. These results suggest that the genomic footprint left by selection on both new and standing variation in strongly bottlenecked populations will be difficult, if not impossible, to find using current approaches.

Evolutionary Biology↗

bioRxiv2014

Synthesizing Combination Therapies for Evolutionary Dynamics of Disease for Nonlinear Pharmacodynamics

Our previous results proposed an iterative scalable algorithm for the systematic design of sparse, small gain feedback strategies that stabilize the evolutionary dynamics of a generic disease model with linear pharmacodynamics. In this manuscript, we use piecewise linear approximations to model nonlinear drug effects. We leverage results from optimal controller synthesis for positive systems to formulate the feedback synthesis problem as an optimization problem that sequentially explores piecewise linear subsystems corresponding to higher and higher treatment dosages.

Evolutionary Biology↗

bioRxiv2014

On the unfounded enthusiasm for soft selective sweeps

Underlying any understanding of the mode, tempo, and relative importance of the adaptive process in the evolution of natural populations is the notion of whether adaptation is mutation-limited. Two very different population genetic models have recently been proposed in which the rate of adaptation is not strongly limited by the rate at which newly arising beneficial mutations enter the population. This review discusses the theoretical underpinnings and requirements of these models, as well as the experimental insights on the parameters of relevance. Importantly, empirical and experimental evidence to date challenges the recent enthusiasm for invoking these models to explain observed patterns of variation in humans and Drosophila.

Evolutionary Biology↗

bioRxiv2014

Human Cytomegalovirus Intrahost Evolution--A New Avenue for Understanding and Controlling Herpesvirus Infections

Human cytomegalovirus (HCMV) is exquisitely adapted to the human host, and much research has focused on its evolution over long timescales spanning millennia. Here, we review recent data exploring the evolution of the virus on much shorter timescales, on the order of days or months. We describe the intrahost genetic diversity of the virus isolated from humans, and how this diversity contributes to HCMV spatiotemporal evolution. We propose mechanisms to explain the high levels of intrahost diversity and discuss how this new information may shed light on HCMV infection and pathogenesis.

Evolutionary Biology↗

bioRxiv2014

Collective action and the collaborative brain

Humans are unique both in their cognitive abilities and in the extent of cooperation in large groups of unrelated individuals. How our species evolved high intelligence in spite of various costs of having a large brain is perplexing. Equally puzzling is how our ancestors managed to overcome the collective action problem and evolve strong innate preferences for cooperative behavior. Here I theoretically study the evolution of social-cognitive competencies as driven by selection emerging from the need to produce public goods in games against nature or in direct competition with other groups. I use collaborative ability in collective actions as a proxy for social-cognitive competencies. My results suggest that collaborative ability is more likely to evolve first by between-group conflicts and then later be utilized and improved in games against nature. If collaborative abilities remain low, the species is predicted to become genetically dimorphic with a small proportion of individuals contributing to public goods and the rest free-riding. Evolution of collaborative ability creates conditions for the subsequent evolution of collaborative communication and cultural learning.

Evolutionary Biology↗

bioRxiv2014

Analysis of geographic patterns of molecular, morphological, and bioclimatic variation to evaluate hypotheses of species boundaries in the South American montane genus Escallonia (Escalloniaceae)

Escallonia is a morphologically and ecologically diverse clade of shrubs and small trees widely distributed in three hotspots of plant diversity. Previous studies suggested that extant species may have radiated rapidly and/or recently resulting in complex patterns of molecular variation across this genus. This result is apparently mirrored in morphology because species also display complex and overlapping patterns of morphological variation. Taken together, these patterns call into question the identity of all species within Escallonia. To evaluate the currently proposed hypotheses of species boundaries, I used molecular, morphological, and bioclimatic a data for 35 species and assessed three species criteria: genealogical exclusivity, morphological gaps, and climatic niche differences. Interpreting these data in the context of species as segments of evolutionary lineages, I provide evidence that most species (ca. 70%) within Escallonia represent distinct species on independent evolutionary trajectories. Instead of rejecting the current hypotheses of species limit, I argue for taxonomic stability as it provides a useful framework for studies aiming to understand the mechanisms driving the origin and evolution of species in hotspots of biodiversity.

Evolutionary Biology↗

bioRxiv2014

Diversifying mechanisms in the on-farm evolution of crop mixtures

While modern agriculture relies on genetic homogeneity in the field, some farmers grow genetically heterogeneous crops and exchange seeds. Such diversifying practices associated with seed recycling may allow adaptation of crops to their environment. This socio-genetical model constitutes an original experimental evolution design called On-Farm Dynamic Management (OFDM). Studying OFDM can help understanding how evolutionary mechanisms shape crop diversity submitted to diverse agro-environmental conditions. We studied a farmer-led initiative where a mixture of four French wheat landraces called \"Melange de Touselles\" (MDT) was created and distributed within a farmers network. Fifteen populations derived by farmers from the initial mixture were sampled after 2 to 7 generations of cultivation on their farm. Twenty-one space-time samples of 80 individuals were genotyped using 17 microsatellites markers and characterized for their heading date in a \"common-garden\" experiment. Gene polymorphism was studied using four markers located in ear-liness genes. An original network-based approach was developed to depict the particular and complex genetic structure of the landraces composing the mixture. A rapid differentiation of the mixture was detected, larger at the phenotypic and gene levels compared to the neutral genetic level, indicating a potential divergent selection. We identified two interacting selection processes: variation of the mixture component frequencies and evolution of the within-variety diversity, that shaped the standing variability available within the mixture. These results confirm that farmers practices increase genetic diversity and allow crop evolution, which is critical in the context of global change. OFDM appears as a promising model of crop experimental evolution.

Evolutionary Biology↗

bioRxiv2014

Reticulate speciation and adaptive introgression in the Anopheles gambiae species complex

Anopheles gambiae, the primary vector of human malaria in sub-Saharan Africa, exists as a series of ecologically specialized subgroups that are phylogenetically nested within the Anopheles gambiae species complex. These species and subgroups exhibit varying degrees of reproductive isolation, sometimes recognized as distinct subspecies. We have sequenced 32 complete genomes from field-captured individuals of Anopheles gambiae, Anopheles gambiae M form (recently named A. coluzzii), sister species A. arabiensis, and the recently discovered \"GOUNDRY\" subgroup of A. gambiae that is highly susceptible to Plasmodium. Amidst a backdrop of strong reproductive isolation and adaptive differentiation, we find evidence for introgression of autosomal chromosomal regions among species and subgroups, some of which have facilitated adaptation. The X chromosome, however, is strongly differentiated among all species and subgroups, pointing to a disproportionately large effect of X chromosome genes in driving speciation among anophelines. Strikingly, we find that autosomal introgression has occurred from contemporary hybridization among A. gambiae and A. arabiensis despite strong divergence ({bsim}5x higher than autosomal divergence) and isolation on the X chromosome. We find a large region of the X chromosome that has swept to fixation in the GOUNDRY subgroup within the last 100 years, which may be an inversion that serves as a partial barrier to contemporary gene flow. We show that speciation with gene flow results in genomic mosaicism of divergence and introgression. Such a reticulate gene pool connecting vector species and subgroups across the speciation continuum has important implications for malaria control efforts.\n\nAuthor SummarySubdivision of species into ecological specialized subgroups allows organisms to access a wider variety of environments and sometimes leads to the formation of species complexes. Adaptation to distinct environments tends to result in differentiation among closely related subgroups, although hybridization can facilitate sharing of globally adaptive alleles. Here, we show that differentiation and hybridization have acted in parallel in a species complex of Anopheles mosquitoes that vector human malaria. In particular, we show that extensive adaptive differentiation and partial reproductive isolation has led to genomic differentiation among mosquito species and subgroups, especially on the X chromosome. However, we also find evidence for exchange of genes on the autosomes that has provided the raw material for recent rapid adaptation. For example, we show that A. arabiensis has shared a mutation conferring insecticide resistance with two subgroups of A. gambiae within the last 60 years, illustrating the fluid nature of species boundaries among even more advanced species pairs. Our results underscore the expected challenges in deploying vector-based disease control strategies since many of the worlds most devastating human pathogens are transmitted by arthropod species complexes.

Evolutionary Biology↗

bioRxiv2014

Scaling properties of evolutionary paths in a biophysical model of protein adaptation

The enormous size and complexity of genotypic sequence space frequently requires consideration of coarse-grained sequences in empirical models. We develop scaling relations to quantify the effect of this coarse-graining on properties of fitness landscapes and evolutionary paths. We first consider evolution on a simple Mount Fuji fitness landscape, focusing on how the length and predictability of evolutionary paths scale with the coarse-grained sequence length and number of alleles. We obtain simple scaling relations for both the weak- and strong-selection limits, with a non-trivial crossover regime at intermediate selection strengths. We apply these results to evolution on a biophysical fitness landscape designed to describe how proteins evolve new binding interactions while maintaining their folding stability. We combine numerical calculations for coarse-grained protein sequences with the scaling relations to obtain quantitative properties of the model for realistic binding interfaces and a full amino acid alphabet.

Evolutionary Biology↗

bioRxiv2014

Quantification of GC-biased gene conversion in the human genome

Many lines of evidence indicate GC-biased gene conversion (gBGC) has a major impact on the evolution of mammalian genomes. However, up to now, this process had not been properly quantified. In principle, the strength of gBGC can be measured from the analysis of derived allele frequency spectra. However, this approach is sensitive to a number of confounding factors. In particular, we show by simulations that the inference is pervasively affected by polymorphism polarization errors, especially at hypermutable sites, and spatial heterogeneity in gBGC strength. Here we propose a new method to quantify gBGC from DAF spectra, incorporating polarization errors and taking spatial heterogeneity into account. This method is very general in that it does not require any prior knowledge about the source of polarization errors and also provides information about mutation patterns. We apply this approach to human polymorphism data from the 1000 genomes project. We show that the strength of gBGC does not differ between hypermutable CpG sites and non-CpG sites, suggesting that in humans gBGC is not caused by the base-excision repair machinery. We further find that the impact of gBGC is concentrated primarily within recombination hotspots: genome-wide, the strength of gBGC is in the nearly neutral area, but 2% of the human genome is subject to strong gBGC, with population-scaled gBGC coefficients above 5. Given that the location of recombination hotspots evolves very rapidly, our analysis predicts that in the long term, a large fraction of the genome is affected by short episodes of strong gBGC.

Evolutionary Biology↗

bioRxiv2014

Species delimitation and phylogeny estimation under the multispecies coalescent

This article describes a Bayesian method for inferring both species delimitations and species trees under the multispecies coalescent model using DNA sequences from multiple loci. The focus here is on species delimitation with no a priori assignment of individuals to species, and no guide tree. The method uses a new model for the population sizes along the branches of the species tree, and three new operators for sampling from the posterior using the Markov chain Monte Carlo (MCMC) algorithm. The correctness of the moves is demonstrated both by proofs and by tests of the implementation. Current practice, using a pipeline approach to species delimitation under the multispecies coalescent, has been shown to have major problems on simulated data [10]. The same simulated data set is used to demonstrate the accuracy and efficiency of the present method. The method is implemented in a package called STACEY for BEAST2.

Evolutionary Biology↗

bioRxiv2014

Massive bursts of transposable element activity in Drosophila

The evolutionary dynamics of transposable element (TE) insertions have been of continued interest since TE activity has important implications for genome evolution and adaptation. Here, we infer the transposition dynamics of TEs by comparing their abundance in natural D. melanogaster and D. simulans populations. Sequencing pools of more than 550 South African flies to at least 320-fold coverage, we determined the genome wide TE insertion frequencies in both species. We show that 46 (49%) TE families in D. melanogaster and 44 (47%) in D. simulans experienced a recent burst of activity. The bursts of activity affected different TE families in the two species. While in D. melanogaster retrotransposons predominated, DNA transposons showed higher activity levels in D. simulans. We propose that the observed TE dynamics are the outcome of the demographic history of the two species, with habitat expansion triggering a period of rapid evolution.

Evolutionary Biology↗