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Results for “Evolutionary Biology”

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bioRxiv2016

Evolutionary thrift: mycobacteria repurpose plasmid diversity during adaptation of type VII secretion systems

Mycobacteria have a distinct secretion system, termed type VII (T7SS), which is encoded by paralogous chromosomal loci (ESX) and associated with pathogenesis, conjugation, and metal homeostasis. Evolution of paralogous gene families is of interest because duplication is an important mechanism by which novel genes evolve, but there are potential conflicts between adaptive forces that stabilize duplications and those that enable evolution of new functions. Our objective was to delineate the adaptive forces underlying diversification of T7SS. Plasmid-borne ESX were described recently, and we found evidence that the initial duplication and divergence of ESX systems occurred on plasmids and was driven by selection for advantageous mutations. Plasmid conjugation has been linked to T7SS and type IV secretion systems (T4SS) in mycobacteria, and we discovered that T7SS and T4SS genes evolved in concert on the plasmids. We hypothesize that differentiation of plasmid ESX helps to prevent conjugation among cells harboring incompatible plasmids. Plasmid ESX appear to have been repurposed following migration to the chromosome, and there is evidence of positive selection driving further differentiation of chromosomal ESX. We hypothesize that ESX loci were initially stabilized on the chromosome by mediating their own transfer. These results emphasize the diverse adaptive paths underlying evolution of novelty, which in this case involved plasmid duplications, selection for advantageous mutations in the mobile and core genomes, migration of the loci between plasmids and chromosomes, and lateral transfer among chromosomes. We discuss further implications for the choice of model organism to study ESX functions in Mycobacterium tuberculosis.

Evolutionary Biology↗

bioRxiv2016

The role of vertical symbiont transmission in altering cooperation and fitness of coral-Symbiodinium symbioses

The coral symbiosis is the linchpin of the reef ecosystem, yet the mechanisms that promote and maintain cooperation between hosts and symbionts have not been fully resolved. We used a phylogenetically controlled design to investigate the role of vertical symbiont transmission, an evolutionary mechanism in which symbionts are inherited directly from parents, predicted to enhance cooperation and holobiont fitness. Six species of coral, three vertical transmitters and their closest horizontally transmitting relatives, which exhibit environmental acquisition of symbionts, were fragmented and subjected to a two-week thermal stress experiment. Symbiont cell density, photosynthetic function and translocation of photosynthetically fixed carbon between symbionts and hosts were quantified to assess changes in physiological performance and cooperation. All species exhibited similar decreases in symbiont cell density and net photosynthesis in response to elevated temperature, consistent with the onset of bleaching. Yet baseline cooperation, i.e. translocation of photosynthate, in ambient conditions and the reduction in cooperation in response to elevated temperature differed among species. Although Porites lobata and Galaxea acrhelia did exhibit the highest levels of baseline cooperation, we did not observe universally higher levels of cooperation in vertically transmitting species. Post hoc sequencing of the Symbiodinium ITS-2 locus was used to investigate the potential role of differences in symbiont community composition. Interestingly, reductions in cooperation at the onset of bleaching tended to be associated with increased symbiont community diversity among coral species. The theoretical benefits of evolving vertical transmission are based on the underlying assumption that the host-symbiont relationship becomes genetically uniform, thereby reducing competition among symbionts. Taken together, our results suggest that it may not be vertical transmission per se that influences host-symbiont cooperation, but genetic uniformity of the symbiont community, although additional work is needed to test this hypothesis.

Evolutionary Biology↗

bioRxiv2016

Beyond Brownian motion and the Ornstein-Uhlenbeck process: Stochastic diffusion models for the evolution of quantitative characters.

Gaussian processes such as Brownian motion and the Ornstein-Uhlenbeck process have been popular models for the evolution of quantitative traits and are widely used in phylogenetic comparative methods. However, they have drawbacks which limit their utility. Here I describe new, non-Gaussian stochastic differential equation (diffusion) models of quantitative trait evolution. I present general methods for deriving new diffusion models, and discuss possible schemes for fitting non-Gaussian evolutionary models to trait data. The theory of stochastic processes provides a mathematical framework for understanding the properties of current, new and future phylogenetic comparative methods. Attention to the mathematical details of models of trait evolution and diversification may help avoid some pitfalls when using stochastic processes to model macroevolution.

Evolutionary Biology↗

bioRxiv2016

Evolution trajectories of snake genes and genomes revealed by comparative analyses of five-pacer viper

Snakes numerous fascinating features distinctive from other tetrapods necessitate a rich history of genome evolution that is still obscure. To address this, we report the first high-quality genome of a viper, Deinagkistrodon acutus and comparative analyses using other species from major snake and lizard lineages. We map the evolution trajectories of transposable elements (TEs), developmental genes and sex chromosomes onto the snake phylogeny. TEs exhibit dynamic lineage-specific expansion. And in the viper many TEs may have been rewired into the regulatory network of brain genes, as shown by their associated expression with nearby genes in the brain but not in other tissues. We detect signatures of adaptive evolution in olfactory, venom and thermal-sensing genes, and also functional degeneration of genes associated with vision and hearing. Many Hox and Tbx limb-patterning genes show evidence of relaxed selective constraints, and such genes phylogenetic distribution supports fossil evidence for a successive loss of forelimbs then hindlimbs during the snake evolution. Finally, we infer that the Z and W sex chromosomes had undergone at least three recombination suppression events at the ancestor of advanced snakes, with the W chromosomes showing a gradient of degeneration from basal to advanced snakes. These results, together with all the genes identified as undergoing adaptive or degenerative evolution episodes at respective snake lineages forge a framework for our deep understanding into snakes molecular evolution history.

Evolutionary Biology↗

bioRxiv2016

rehh 2.0: a reimplementation of the R package rehh to detect positive selection from haplotype structure.

Identifying genomic regions with unusually high local haplotype homozygosity represents a powerful strategy to characterize candidate genes responding to natural or artificial positive selection. To that end, statistics measuring the extent of haplotype homozygosity within (e.g., EHH, iHS) and between (Rsb or XP-EHH) populations have been proposed in the literature. The O_SCPLOWREHHC_SCPLOW package for R was previously developed to facilitate genome-wide scans of selection, based on the analysis of long-range haplotypes. However, its performance wasnt sufficient to cope with the growing size of available data sets. Here we propose a major upgrade of the O_SCPLOWREHHC_SCPLOW package, which includes an improved processing of the input files, a faster algorithm to enumerate haplotypes, as well as multi-threading. As illustrated with the analysis of large human haplotype data sets, these improvements decrease the computation time by more than an order of magnitude. This new version of O_SCPLOWREHHC_SCPLOW will thus allow performing iHS-, Rsb- or XP-EHH-based scans on large data sets. The package O_SCPLOWREHHC_SCPLOW 2.0 is available from the CRAN repository (http://cran.r-project.org/web/packages/rehh/index.html) together with help files and a detailed manual.

Evolutionary Biology↗

bioRxiv2016

Pollutants and insecticides drive local adaptation in African malaria mosquitoes

The Anopheles gambiae complex contains a number of highly anthropophilic mosquito species that have acquired exceptional ability to thrive in complex human habitats. Thus, examining the evolutionary history of this Afrotropical mosquito may yield vital information on the selective processes that occurred during the adaptation to human-dominated environments. We performed reduced representation sequencing on 941 mosquitoes of the Anopheles gambiae complex collected across four ecogeographic zones in Cameroon. We find evidence for genetic and geographic subdivision within An. coluzzii and An. gambiae sensu stricto - the two most significant malaria vectors in the region. Importantly, in both species, rural and urban populations are genetically differentiated. Genome scans reveal pervasive signatures of selection centered on genes involved in xenobiotic resistance. Notably, a selective sweep containing detoxification enzymes is prominent in urban mosquitoes that exploit polluted breeding sites. Overall, our study suggests that recent anthropogenic environmental modifications and widespread use of insecticides are driving population differentiation and local adaptation in vectors with potentially significant consequences for malaria epidemiology.

Evolutionary Biology↗

bioRxiv2016

Genetic Diversity, Population Structure and Species Delimitation of Trialeurodes vaporariorum (Greenhouse whitefly)

Genetic diversity within Trialeurodes vaporariorum (Westwood, 1856) remains largely unexplored, particularly within regions of Sub-Saharan Africa. In this study, T. vaporariorum samples were obtained from three locations in Kenya: Katumani, Kiambu and Kajiado counties. DNA extraction, PCR and Sanger sequencing were carried out on ~750 bp fragment of the mitochondria cytochrome c oxidase I (COI) gene from individual whiteflies. In addition, global populations were assessed and 19 haplotypes were identified, with three main haplotypes (Hp_19, Hp_10, Hp_011) circulating within Kenya. Measures of genetic diversity among T. vaporariorum populations resulted in haplotype diversity of 0.411, nucleotide diversity 0.00096, and Tajimas D -0. 30315, (P>0.10). Analysis of population structure across global sequences using Structurama indicated one population globally, with posterior probability of 0.72. Bayesian and maximum likelihood phylogenetic analysis gave support for two clades (Clade I = an admixed global population and Clade II = subset of Kenyan and 1 Greek sequence). Species delimitation between the two clades was assessed by four parameters; posterior probability, Kimuras two parameter (K2P), Rodrigos P (Randomly distinct) and Rosenbergs reciprocal monophyly (P(AB). The two clades within the phylogenetic tree showed evidence of distinctness based on; Kimura two parameters (K2P) (p = -1.21E-01), Rodrigos P (RD) (p =0.05) and Rosenbergs P(AB) (p = 2.3E -13). Overall, low genetic diversity within the Kenyan samples is a likely indicator of recent population expansion and colonization with this region and plausible signs of species complex formation in Sub-Saharan Africa.

Evolutionary Biology↗

bioRxiv2016

Recombination-driven genome evolution and stability of bacterial species

While bacteria divide clonally, horizontal gene transfer followed by homologous recombination is now recognized as an important and sometimes even dominant contributor to their evolution. However, the details of how the competition between clonal inheritance and recombination shapes genome diversity, population structure, and species stability remains poorly understood. Using a computational model, we find two principal regimes in bacterial evolution and identify two composite parameters that dictate the evolutionary fate of bacterial species. In the divergent regime, characterized by either a low recombination frequency or strict barriers to recombination, cohesion due to recombination is not sufficient to overcome the mutational drift. As a consequence, the divergence between any pair of genomes in the population steadily increases in the course of their evolution. The species as a whole lacks genetic coherence with sexually isolated clonal sub-populations continuously formed and dissolved. In contrast, in the metastable regime, characterized by a high recombination frequency combined with low barriers to recombination, genomes continuously recombine with the rest of the population. The population remains genetically cohesive and stable over time. The transition between these two regimes can be affected by relatively small changes in evolutionary parameters. Using the Multi Locus Sequence Typing (MLST) data we classify a number of well-studied bacterial species to be either the divergent or the metastable type. Generalizations of our framework to include fitness and selection, ecologically structured populations, and horizontal gene transfer of non-homologous regions are discussed.

Evolutionary Biology↗

bioRxiv2016

Evolution of simple multicellularity increases environmental complexity

Multicellularity--the integration of previously autonomous cells into a new, more complex organism--is one of the major transitions in evolution. Multicellularity changed evolutionary possibilities and facilitated the evolution of increased complexity. Transitions to multicellularity are associated with rapid diversification and increased ecological opportunity but the potential mechanisms are not well understood. In this paper we explore the ecological mechanisms of multicellular diversification during experimental evolution of the brewers yeast, Saccharomyces cerevisiae. The evolution from single cells into multicellular clusters modifies the structure of the environment, changing the fluid dynamics and creating novel ecological opportunities. This study demonstrates that even in simple conditions, incipient multicellularity readily changes the environment, facilitating the origin and maintenance of diversity.

Evolutionary Biology↗

bioRxiv2016

Testing for local adaptation and evolutionary potential along altitudinal gradients in rainforest Drosophila: limitations of laboratory estimates.

Predicting how species will respond to the rapid climatic changes predicted this century is an urgent task. Species Distribution Models (SDMs) use the current relationship between environmental variation and species abundances to predict the effect of future environmental change on their distributions. However, two common assumptions of SDMs are likely to be violated in many cases: (1) that the relationship of environment with abundance or fitness is constant throughout a species range and will remain so in future, and (2) that abiotic factors (e.g. temperature, humidity) determine species distributions. We test these assumptions by relating field abundance of the rainforest fruit fly Drosophila birchii to ecological change across gradients that include its low and high altitudinal limits. We then test how such ecological variation affects the fitness of 35 D. birchii families transplanted in 591 cages to sites along two altitudinal gradients, to determine whether genetic variation in fitness responses could facilitate future adaptation to environmental change. Overall, field abundance was highest at cooler, high altitude sites, and declined towards warmer, low altitude sites. By contrast, cage fitness (productivity) increased towards warmer, lower altitude sites, suggesting that biotic interactions (absent from cages) drive ecological limits at warmer margins. In addition, the relationship between environmental variation and abundance varied significantly among gradients, indicating divergence in ecological niche across the species range. However, there was no evidence for local adaptation within gradients, despite greater productivity of high altitude than low altitude populations when families were reared under laboratory conditions. Families also responded similarly to transplantation along gradients, providing no evidence for fitness trade-offs that would favour local adaptation. These findings highlight the importance of (1) measuring genetic variation of key traits under ecologically relevant conditions, and (2) considering the effect of biotic interactions when predicting species responses to environmental change.

Evolutionary Biology↗

bioRxiv2016

Chromosomal inversions facilitate chromosome-scale evolution in Anopheles funestus

Chromosomal inversions facilitate local adaptation of beneficial mutations and modulate genetic polymorphism, but the extent of their effects within the genome is still insufficiently understood. The genome of Anopheles funestus, a malaria mosquito endemic to sub-Saharan Africa, contains an impressive number of paracentric polymorphic inversions, which are unevenly distributed among chromosomes and provide an excellent framework for investigating the genomic impacts of chromosomal rearrangements. Here we present results of a fine-scale analysis of genetic variation within the genome of two weakly differentiated populations of Anopheles funestus inhabiting contrasting moisture conditions in Cameroon. Using population genomic analyses, we found that genetic divergence between the two populations is centered on regions of the genome corresponding to three inversions, which are characterized by high values of FST, absolute sequence divergence and fixed differences. Importantly, in contrast to the 2L chromosome arm, which is collinear, nucleotide diversity is significantly reduced along the entire length of three autosome arms bearing multiple overlapping chromosomal rearrangements. These findings support the idea that interactions between reduced recombination and natural selection within inversions contribute to sculpt nucleotide polymorphism across chromosomes in An. funestus.

Evolutionary Biology↗

bioRxiv2016

Rapid expansion of immune-related gene families in the house fly, Musca domestica

The house fly, Musca domestica, occupies an unusual diversity of potentially septic niches among sequenced Dipteran insects and is a vector of numerous diseases of humans and livestock. In the present study, we apply whole-transcriptome sequencing to identify genes whose expression is regulated in adult flies by bacterial infection. We then combine the transcriptomic data with analysis of rates of gene duplication and loss to provide insight into the evolutionary dynamics of immune-related genes. Genes up-regulated after bacterial infection are biased toward being evolutionarily recent innovations, suggesting the recruitment of novel immune components in the M. domestica or ancestral Dipteran lineages. In addition, using new models of gene family evolution, we show that several different classes of immune-related genes, particularly those involved in either pathogen recognition or pathogen killing, are duplicating at a significantly accelerated rate on the M. domestica lineage relative to other Dipterans. Taken together, these results suggest that the M. domestica immune response includes an unusual diversity of genes, perhaps as a consequence of its lifestyle in septic environments.

Evolutionary Biology↗

bioRxiv2016

Genomic signatures of introgression at late stages of speciation in a malaria mosquito

Ongoing speciation in most African malaria vectors gives rise to cryptic populations, which differ remarkably in their behaviour, ecology and capacity to vector malaria parasites. Understanding the population structure and the drivers of genetic differentiation among mosquitoes is critical for effective disease control because heterogeneity within species contribute to variability in malaria cases and allow fractions of vector populations to escape control efforts. To examine the population structure and the potential impacts of recent large-scale control interventions, we have investigated the genomic patterns of differentiation in mosquitoes belonging to the Anopheles nili group, a large taxonomic group that diverged [~]3-Myr ago. Using 4343 single nucleotide polymorphisms (SNPs), we detected strong population structure characterized by high FST values between multiple divergent populations adapted to different habitats within the Central African rainforest. Delineating the cryptic species within the Anopheles nili group is challenging due to incongruence between morphology, ribosomal DNA and SNP markers consistent with incomplete lineage sorting and/or interspecific gene flow. A very high proportion of loci are fixed (FST = 1) within the genome of putative species, which suggests that ecological and/or reproductive barriers are maintained by strong selection on a substantial number of genes.

Evolutionary Biology↗

bioRxiv2016

Extensive genetic diversity among populations of the malaria mosquito Anopheles moucheti revealed by population genomics

Malaria vectors are exposed to intense selective pressures due to large-scale intervention programs that are underway in most African countries. One of the current priorities is therefore to clearly assess the adaptive potential of Anopheline populations, which is critical to understand and anticipate the response mosquitoes can elicit against such adaptive challenges. The development of genomic resources that will empower robust examinations of evolutionary changes in all vectors including currently understudied species is an inevitable step toward this goal. Here we constructed double-digest Restriction Associated DNA (ddRAD) libraries and generated 6461 Single Nucleotide Polymorphisms (SNPs) that we used to explore the population structure and demographic history of wild-caught Anopheles moucheti from Cameroon. The genome-wide distribution of allelic frequencies among samples best fitted that of an old population at equilibrium, characterized by a weak genetic structure and extensive genetic diversity, presumably due to a large long term effective population size. Estimates of FST and Linkage Disequilibrium (LD) across SNPs reveal a very low genetic differentiation throughout the genome and the absence of segregating LD blocks among populations, suggesting an overall lack of local adaptation. Our study provides the first investigation of the genetic structure and diversity in An. moucheti at the genomic scale. We conclude that, despite a weak genetic structure, this species has the potential to challenge current vector control measures and other rapid anthropogenic and environmental changes thanks to its great genetic diversity.

Evolutionary Biology↗

bioRxiv2016

Dynamics and fate of beneficial mutations under lineage contamination by linked deleterious mutations

Beneficial mutations drive adaptive evolution, yet their selective advantage does not ensure their fixation. Haldanes application of single-type branching process theory showed that genetic drift alone could cause the extinction of newly-arising beneficial mutations with high probability. With linkage, deleterious mutations will affect the dynamics of beneficial mutations and might further increase their extinction probability. Here, we model the lineage dynamics of a newly-arising beneficial mutation as a multitype branching process; this approach allows us to account for the combined effects of drift and the stochastic accumulation of linked deleterious mutations, which we call lineage contamination. We first study the lineage contamination phenomenon in isolation, deriving extinction times and probabilities of beneficial lineages. We then put the lineage contamination phenomenon into the context of an evolving population by incorporating the effects of background selection. We find that the survival probability of beneficial mutations is simply Haldanes classical formula multiplied by the correction factor [Formula], where U is deleterious mutation rate, [Formula] is mean selective advantage of beneficial mutations,{kappa} [isin] (1,{varepsilon} ], and{varepsilon} = 2 - e-1. We also find there exists a genomic deleterious mutation rate, [Formula], that maximizes the rate of production of surviving beneficial mutations, and that [Formula]. Both of these results, and others, are curiously independent of the fitness effects of deleterious mutations. We derive critical mutation rates above which: 1) lineage contamination alleviates competition among beneficial mutations, and 2) the adaptive substitution process all but shuts down.

Evolutionary Biology↗

bioRxiv2016

Population structure reduces the benefits from partner choice in mutualism

Mutualisms are key drivers of evolutionary and ecological processes. Understanding how different species can evolve to interact in mutually beneficial ways is an important goal of evolutionary theory, especially when the benefits require costly investments by the partners. For such costly investments to evolve, some sort of fitness feedback mechanism must exist that more than recoups the direct costs. Several such feedback mechanisms have been explored both theoretically and empirically, yet we know relatively little how they might act together, as they probably do in nature. In this paper, I model the joint action of three of the main mechanisms that can maintain symbiotic cooperation: partner choice by hosts, population structure amongst symbionts, and undirected rewards from hosts to symbionts. My results show that population structure reduces the benefit from partner choice to hosts. It may help or hinder beneficial symbionts and create positive or negative frequency dependence depending on the nature of host rewards to the symbiont. Strong population structure also makes it less likely that host choosiness and symbiont cooperation will be jointly maintained in a population. The intuition behind my results is that all else being equal, population structure reduces local variation available to the host to choose from. Thus, population structure is not always beneficial for the evolution of cooperation between species. My results also underscore the need to do full analyses of multiple mechanisms of social evolution to uncover their interactions to uncover the interactions between them.

Evolutionary Biology↗

bioRxiv2016

The frequency spectrum of chromatin accessibility in Yorubans points toward a significant role of random genetic drift in shaping the chromatin landscape

The function of non-coding variation in the human genome is hotly debated. While much of the genome appears to be involved in some kind of molecular activity, a relatively small portion of the genome appears to be conserved across mammalian species. To try to understand part of this seeming paradox, we examined chromatin accessibility as a model molecular phenotype. We modeled chromatin state as either open or closed as looked at the frequency of open chromatin across 70 Yoruban cell lines. We saw that most regions of chromatin accessibility occurred in only a small number of individuals, although there are a number of regions that are accessible across the entire panel. To delve further into understanding the evolutionary mechanisms, we examined nucleotide diversity in and around accessible regions. We found that in the open chromatin access, low frequency regions had decreased nucleotide diversity, however, they were situated within regions of elevated nucleotide diversity. These results point toward a role of random mutation and genetic drift shaping the distribution of accessible regions in the human genome.

Evolutionary Biology↗

bioRxiv2016

Modeling the multiple facets of speciation-with-gene-flow towards improving divergence history inference of a recent fish adaptive radiation.

Parallel divergence patterns across replicated species pairs occurring in similar environmental contrasts may arise through distinct evolutionary scenarios. Deciphering whether such parallelism actually reflects repeated parallel divergence driven by divergent selection or a single divergence event with subsequent gene flow needs to be ascertained. Reconstructing historical gene flow is therefore of fundamental interest to understand how demography and selection jointly shaped genomic divergence during speciation. Here, we use an extended modeling framework to explore the multiple facets of speciation-with-gene-flow with demo-genetic divergence models that capture both temporal and genomic variation in effective population size and migration rate. We investigate the divergence history of five sympatric Lake Whitefish limnetic (dwarf) and benthic (normal) species pairs characterized by variable degrees of ecological divergence and reproductive isolation. Genome-wide SNPs were used to document the extent of genetic differentiation in each species pair, and 26 divergence models were fitted and compared to the unfolded joint allele frequency spectrum of each pair. We found evidence that a recent (circa 3000-4000 generations) asymmetrical secondary contact between expanding post-glacial populations has accompanied Whitefish diversification. Our results suggest that heterogeneous genomic differentiation patterns have emerged through the combined effects of linked selection generating variable rates of lineage sorting across the genome during geographical isolation, and heterogeneous introgression eroding divergence at different rates across the genome upon secondary contact. This study thus provides a new retrospective insight into the historical demographic and selective processes that shaped a continuum of divergence associated with ecological speciation.

Evolutionary Biology↗