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bioRxiv2016

Minimal-assumption inference from population-genomic data

Samples of multiple complete genome sequences contain vast amounts of information about the evolutionary history of populations, much of it in the associations among polymorphisms at different loci. Current methods that take advantage of this linkage information rely on models of recombination and coalescence, limiting the sample sizes and populations that they can analyze. We introduce a method, Minimal-Assumption Genomic Inference of Coalescence (MAGIC), that reconstructs key features of the evolutionary history, including the distribution of coalescence times, by integrating information across genomic length scales without using an explicit model of recombination, demography or selection. Using simulated data, we show that MAGICs performance is comparable to PSMC on single diploid samples generated with standard coalescent and recombination models. More importantly, MAGIC can also analyze arbitrarily large samples and is robust to changes in the coalescent and recombination processes. Using MAGIC, we show that the inferred coalescence time histories of samples of multiple human genomes exhibit inconsistencies with a description in terms of an effective population size based on single-genome data.

evolutionary biology↗

bioRxiv2016

Ploidy tug-of-war: evolutionary and genetic environments influence the rate of ploidy drive in a human fungal pathogen

Variation in baseline ploidy is seen throughout the tree of life, yet the factors that determine why one ploidy level is selected over another remain poorly understood. Experimental evolution studies using asexual fungal microbes with manipulated ploidy levels intriguingly reveals a propensity to return to the historical baseline ploidy, a phenomenon that we term ploidy drive. We evolved haploid, diploid, and polyploid strains of the human fungal pathogen Candida albicans under three different nutrient limitation environments to test whether these conditions, hypothesized to select for low ploidy levels, could counteract ploidy drive. Strains generally maintained or acquired smaller genome sizes in minimal medium and under phosphorus depletion compared to in a complete medium, while mostly maintained or acquired increased genome sizes under nitrogen depletion. Surprisingly, improvements in fitness often ran counter to changes in total nuclear genome size; in a number of scenarios lines that maintained their original genome size often increased in fitness more than lines that converged towards diploidy. Combined, this work demonstrates a role for both the environment and genotype in determination of the rate of ploidy drive, and highlights questions that remain about the force(s) that cause genome size variation.

evolutionary biology↗

bioRxiv2016

Vertically transmitted rhabdoviruses are found across three insect families and have dynamic interactions with their hosts

A small number of free-living viruses have been found to be obligately vertically transmitted, but it remains uncertain how widespread vertically transmitted viruses are and how quickly they can spread through host populations. Recent metagenomic studies have found several insects to be infected with sigma viruses (Rhabdoviridae). Here, we report that sigma viruses that infect Mediterranean fruit flies (Ceratitis capitata), Drosophila immigrans, and speckled wood butterflies (Pararge aegeria) are all vertically transmitted. We find patterns of vertical transmission that are consistent with those seen in Drosophila sigma viruses, with high rates of maternal transmission, and lower rates of paternal transmission. This mode of transmission allows them to spread rapidly in populations, and using viral sequence data we found the viruses in D. immigrans and C. capitata had both recently swept through host populations. The viruses were common in nature, with mean prevalences of 12% in C. capitata, 38% in D. immigrans and 74% in P. aegeria. We conclude that vertically transmitted rhabdoviruses may be widespread in insects, and that these viruses can have dynamic interactions with their hosts.

evolutionary biology↗

bioRxiv2016

The natural selection of metabolism and mass selects allometric transitions from prokaryotes to mammals

Inter-specific body mass allometries can evolve from the natural selection of mass, with {+/-}1/4 and {+/-}3/4 exponents following from the geometry of intra-specific interactions when density dependent foraging occurs in two spatial dimensions (2D, Witting, 1995). The corresponding values for three dimensional interactions (3D) are {+/-}1/6 and {+/-}5/6.\n\nBut the allometric exponents in mobile organisms are more diverse than the prediction. The exponent for mass specific metabolism tends to cluster around -1/4 and -1/6 in terrestrial and pelagic vertebrates, but it is strongly positive in prokaryotes with an apparent value around 5/6 (DeLong et al., 2010). And a value around zero has been reported in protozoa, and on the macro evolutionary scale from prokaryotes over larger unicells to multicellular vertebrates (Makarieva et al., 2005, 2008).\n\nI show that mass specific metabolism can be selected as the pace of the resource handling that generates net energy for self-replication and the selection of mass, and that this selection of metabolism and mass is sufficient to explain metabolic exponents that decline from 5/6 over zero to -1/6 in 3D, and from 3/4 over zero to -1/4 in 2D. The decline follows from a decline in the importance of mass specific metabolism for the selection of mass, and it suggests i) that the body mass variation in prokaryotes is selected from primary variation in mass specific metabolism, ii) that the variation in multicellular animals are selected from primary variation in the handling and/or densities of the underlying resources, iii) that protozoa are selected as an intermediate lifeform between prokaryotes and multicellular animals, and iv) that macro evolution proceeds along an upper bound on mass specific metabolism.

evolutionary biology↗

bioRxiv2016

Habitat preference predicts genetic diversity and population divergence in Amazonian birds

The ecological traits of organisms may predict important evolutionary parameters such as genetic diversity, population genetic structure, and demographic history. Making these ecological-evolutionary links is difficult because robust, comparable genetic estimates are required from many species with differing ecologies. In Amazonian birds, differences in habitat preference are an important component of ecological diversity. A subset of Amazonian birds is restricted to forest edge and open forest along floodplains, whereas another subset occurs only in the interior of tall, upland forest. Here, we examine the link between habitat and evolutionary metrics using 20 pairs of closely related and co-distributed bird species in which one member of the pair occurs primarily in forest edge and floodplains, and the other occurs in upland forest interior. We use standardized geographic sampling and genomic data from the same set of 2,416 independent markers to estimate genetic diversity, population structure, and demographic history in each species. We find that species of upland forest have higher genetic diversity, greater divergence across the landscape, more genetically distinct populations, and deeper gene histories than floodplain species. Our results reveal that species ecology in the form of habitat preference is an important predictor of genetic diversity and divergence and suggest that floodplain and upland avifaunas in the Amazon may be on separate evolutionary trajectories and require different conservation strategies.

evolutionary biology↗

bioRxiv2016

Inferring the role of habitat dynamics in driving diversification: evidence for a species pump in Lake Tanganyika cichlids

Geographic isolation that drives speciation is often assumed to slowly increase over time, for instance through the formation of rivers, the formation of mountains or the movement of tectonic plates. Cyclic changes in connectivity between areas may occur with the advancement and retraction of glaciers, with water level fluctuations in seas between islands or in lakes that have an uneven bathymetry. These habitat dynamics may act as a driver of allopatric speciation and propel local diversity. Here we present a parsimonious model of the interaction between cyclical (but not necessarily periodic) changes in the environment and speciation, and provide an ABC-SMC method to infer the rates of allopatric and sympatric speciation from a phylogenetic tree. We apply our approach to the posterior sample of an updated phylogeny of the Lamprologini, a tribe of cichlid fish from Lake Tanganyika where such cyclic changes in water level have occurred. We find that water level changes play a crucial role in driving diversity in Lake Tanganyika. We note that if we apply our analysis to the Most Credible Consensus (MCC) tree, we do not find evidence for water level changes influencing diversity in the Lamprologini, suggesting that the MCC tree is a misleading representation of the true species tree. Furthermore, we note that the signature of habitat dynamics is found in the posterior sample despite the fact that this sample was constructed using a species tree prior that ignores habitat dynamics. However, in other cases this species tree prior might erase this signature. Hence we argue that in order to improve inference of the effect of habitat dynamics on biodiversity, phylogenetic reconstruction methods should include tree priors that explicitly take into account such dynamics.

evolutionary biology↗

bioRxiv2016

Phylogenetic relationships and genome size evolution within the genus Amaranthus indicate the ancestors of an ancient crop

The genus Amaranthus consists of 50 to 70 species and harbors several cultivated and weedy species of great economic importance. A small number of suitable traits, phenotypic plasticity, gene flow and hybridization made it difficult to establish the taxonomy and phylogeny of the whole genus despite various studies using molecular markers. We inferred the phylogeny of the Amaranthus genus using genotyping by sequencing (GBS) of 94 genebank accessions representing 35 Amaranthus species and measured their genome sizes. SNPs were called by de novo and reference-based methods, for which we used the distant sugarbeet Beta vulgaris and the closely related Amaranthus hypochondriacus as references. SNP counts and proportions of missing data differed between methods, but the resulting phylogenetic trees were highly similar. A distance-based neighbor joing tree of individual accessions and a species tree calculated with the multispecies coalescent supported a previous taxonomic classification into three subgenera although the subgenus A. Acnida consists of two highly differentiated clades. The analysis of the Hybridus complex within the A. Amaranthus subgenus revealed insights on the history of cultivated grain amaranths. The complex includes the three cultivated grain amaranths and their wild relatives and was well separated from other species in the subgenus. Wild and cultivated amaranth accessions did not differentiate according to the species assignment but clustered by their geographic origin from South and Central America. Different geographically separated populations of Amaranthus hybridus appear to be the common ancestors of the three cultivated grain species and A. quitensis might be additionally be involved in the evolution of South American grain amaranth (A. caudatus). We also measured genome sizes of the species and observed little variation with the exception of two lineages that showed evidence for a recent polyploidization. With the exception of two lineages, genome sizes are quite similar and indicate that polyploidization did not play a major role in the history of the genus.

evolutionary biology↗

bioRxiv2016

Phylogenetic analysis suggests joint control of transmission mode in a grass-endophyte symbiosis

How symbionts are transmitted between hosts is key to determining whether symbioses evolve to be harmful or beneficial. Vertical transmission favors mutualistic symbionts, and horizontal transmission more virulent ones. Transmission mode evolution itself depends on whether the host or symbiont can respond to selection on transmission mode. When hosts control the transmission mode, vertical transmission should evolve under more restrictive circumstances than when symbionts are in control. We take a phylogenetic approach to determine whether the host, symbiont, or both control transmission mode using the pooid grass-epichloid endophyte symbiosis as a model system. This study is the first to investigate control of transmission mode evolution in a phylogenetic context. We find a signal of host phylogeny but only in conjunction with symbiont identity. This pattern suggests joint control of transmission mode by the host and symbiont. It also suggests that non-genetic or non-conserved symbiont traits may determine whether host traits lead to vertical or horizontal transmission.

evolutionary biology↗

bioRxiv2016

Identifying genetic variants that affect viability in large cohorts

A number of open questions in human evolutionary genetics would become tractable if we were able to directly measure evolutionary fitness. As a step towards this goal, we developed a method to examine whether individual genetic variants, or sets of genetic variants, currently influence viability. The approach consists in testing whether the frequency of an allele varies across ages, accounting for variation in ancestry. We applied it to the Genetic Epidemiology Research on Aging (GERA) cohort and to the parents of participants in the UK Biobank. Across the genome, we find only a few common variants with large effects on age-specific mortality: tagging the APOE {varepsilon}4 allele and near CHRNA3. These results suggest that when large, even late onset effects are kept at low frequency by purifying selection. Testing viability effects of sets of genetic variants that jointly influence one of 42 traits, we detect a number of strong signals. In participants of the UK Biobank study of British ancestry, we find that variants that delay puberty timing are enriched in longer-lived parents (P~6x10-6 for fathers and P~2x10-3 for mothers), consistent with epidemiological studies. Similarly, in mothers, variants associated with later age at first birth are associated with a longer lifespan (P~1x10-3). Signals are also observed for variants influencing cholesterol levels, risk of coronary artery disease, body mass index, as well as risk of asthma. These signals exhibit consistent effects in the GERA cohort and among participants of the UK Biobank of non-British ancestry. Moreover, we see marked differences between males and females, most notably at the CHRNA3 locus, and variants associated with risk of coronary artery disease and cholesterol levels. Beyond our findings, the analysis serves as a proof of principle for how upcoming biomedical datasets can be used to learn about selection effects in contemporary humans.

evolutionary biology↗

bioRxiv2016

Estimation of sub-epidemic dynamics by means of Sequential Monte Carlo Approximate Bayesian Computation: an application to the Swiss HIV Cohort Study

Our ability to accurately infer transmission patterns of infectious diseases is critical to monitor both their spread and the efficacy of public health policies. The use of phylogenetic methods for the reconstruction of viral ancestral relationships has garnered increasing interest, particularly in the characterization of HIV epidemics and sub-epidemics. In the case of this virus, the Swiss HIV Cohort Study (SHCS) contains a wide breadth of genomic data that have been widely used as a means of applying such methods. However, current approaches for quantifying the epidemiological dynamics of diseases are computationally intensive, and fail to scale well with this magnitude of data. To address this issue, we re-implement an Approximate Bayesian Computation (ABC) approach based on sequential Monte Carlo (SMC). By means of simulations, we demonstrate that our implementation is capable of inferring key epidemiological parameters of the Swiss HIV epidemic accurately, and that sampling intensity has no significant effect on the accuracy of our estimates. Applied to a subset of HIV sequences from the SHCS, we show that we can distinguish sub-epidemics that are circulating in culturally distinct Swiss regions. Given these findings, we propose that ABC-SMC samplers will allow us to evaluate the impact of new public health policies, such as the implementation of a needle exchange program in the case of HIV, based on genetic data sampled before and after the implementation of a new policy.

evolutionary biology↗

bioRxiv2016

Rapid and recent evolution of LTR retrotransposons drives rice genome evolution during the speciation of AA- genome Oryza species

The dynamics of LTR retrotransposons and their contribution to genome evolution during plant speciation have remained largely unanswered. Here, we perform a genome-wide comparison of all eight Oryza AA- genome species, and identify 3,911 intact LTR retrotransposons classified into 790 families. The top 44 most abundant LTR retrotransposon families show patterns of rapid and distinct diversification since the species split over the last ~4.8 Myr. Phylogenetic and read depth analyses of 11 representative retrotransposon families further provide a comprehensive evolutionary landscape of these changes. Compared with Ty1-copia, independent bursts of Ty3-gypsy retrotransposon expansions have occurred with the three largest showing signatures of lineage-specific evolution. The estimated insertion times of 2,213 complete retrotransposons from the top 23 most abundant families reveal divergent life-histories marked by speedy accumulation, decline and extinction that differed radically between species. We hypothesize that this rapid evolution of LTR retrotransposons not only divergently shaped the architecture of rice genomes but also contributed to the process of speciation and diversification of rice.

evolutionary biology↗

bioRxiv2016

Direct estimation of the spontaneous mutation rate by short-term mutation accumulation lines in Chironomus riparius

Mutations are the ultimate basis of evolution, yet their occurrence rate is known only for few species. We directly estimated the spontaneous mutation rate and the mutational spectrum in the non-biting midge C. riparius with a new approach. Individuals from ten mutation accumulation lines over five generations were deep genome sequenced to count de novo mutations (DNMs) that were not present in a pool of F1 individuals, representing parental genotypes. We identified 51 new single site mutations of which 25 were insertions or deletions and 26 single point mutations. This shift in the mutational spectrum compared to other organisms was explained by the high A/T content of the species. We estimated a haploid mutation rate of 2.1 x 10-9 (95% confidence interval: 1.4 x 10-9 - 3.1 x 10-9) which is in the range of recent estimates for other insects and supports the drift barrier hypothesis. We show that accurate mutation rate estimation from a high number of observed mutations is feasible with moderate effort even for non-model species.

evolutionary biology↗

bioRxiv2016

Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts

Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long-term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement and/or supplementation of an obligate symbiosis by an additional bacterium has occurred during the history of many insect groups. Yet, the factors favoring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a \"menage a trois\", in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species+confirm that these coresident symbionts fulfill essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that co-symbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.

evolutionary biology↗

bioRxiv2016

Evolutionary forces affecting synonymous variations in plant genomes

Base composition is highly variable among and within plant genomes, especially at third codon positions, ranging from GC-poor and homogeneous species to GC-rich and highly heterogeneous ones (particularly Monocots). Consequently, synonymous codon usage is biased in most species, even when base composition is relatively homogeneous. The causes of these variations are still under debate, with three main forces being possibly involved: mutational bias, selection and GC-biased gene conversion (gBGC). So far, both selection and gBGC have been detected in some species but how their relative strength varies among and within species remains unclear. Population genetics approaches allow to jointly estimating the intensity of selection, gBGC and mutational bias. We extended a recently developed method and applied it to a large population genomic datasets based on transcriptome sequencing of 11 angiosperm species spread across the phylogeny. We found that base composition is far from mutation-drift equilibrium in most genomes and that gBGC is a widespread and stronger process than selection. gBGC could strongly contribute to base composition variation among plant species, implying that it should be taken into account in plant genome analyses, especially for GC-rich ones.

evolutionary biology↗

bioRxiv2016

Anchored Phylogenomics of Angiosperms I: Assessing the Robustness of Phylogenetic Estimates

An important goal of the angiosperm systematics community has been to develop a shared approach to molecular data collection, such that phylogenomic data sets from different focal clades can be combined for meta-studies across the entire group. Although significant progress has been made through efforts such as DNA barcoding, transcriptome sequencing, and whole-plastid sequencing, the community current lacks a cost efficient methodology for collecting nuclear phylogenomic data across all angiosperms. Here, we leverage genomic resources from 43 angiosperm species to develop enrichment probes useful for collecting ~500 loci from non-model taxa across the diversity of angiosperms. By taking an anchored phylogenomics approach, in which probes are designed to represent sequence diversity across the group, we are able to efficiently target loci with sufficient phylogenetic signal to resolve deep, intermediate, and shallow angiosperm relationships. After demonstrating the utility of this resource, we present a method that generates a heat map for each node on a phylogeny that reveals the sensitivity of support for the node across analysis conditions, as well as different locus, site, and taxon schemes. Focusing on the effect of locus and site sampling, we use this approach to statistically evaluate relative support for the alternative relationships among eudicots, monocots, and magnoliids. Although the results from supermatrix and coalescent analyses are largely consistent across the tree, we find support for this deep relationship to be more sensitive to the particular choice of sites and loci when a supermatrix approach as employed. Averaged across analysis approaches and data subsampling schemes, our data support a eudicot-monocot sister relationship, which is supported by a number of recent angiosperm studies.

evolutionary biology↗

bioRxiv2016

Biased gene conversion drives codon usage in human and precludes selection on translation efficiency

In humans, as in other mammals, synonymous codon usage (SCU) varies widely among genes. In particular, genes involved in cell differentiation or in proliferation display a distinct codon usage, suggesting that SCU is adaptively constrained to optimize translation efficiency in distinct cellular states. However, in mammals, SCU is known to correlate with large-scale fluctuations of GC-content along chromosomes, caused by meiotic recombination, via the non-adaptive process of GC-biased gene conversion (gBGC). To disentangle and to quantify the different factors driving SCU in humans, we analyzed the relationships between functional categories, base composition, recombination, and gene expression. We first demonstrate that SCU is predominantly driven by large-scale variation in GC-content and is not linked to constraints on tRNA abundance, which excludes an effect of translational selection. In agreement with the gBGC model, we show that differences in SCU among functional categories are explained by variation in intragenic recombination rate, which, in turn, is strongly negatively correlated to gene expression levels during meiosis. Our results indicate that variation in SCU among functional categories (including variation associated to differentiation or proliferation)- result from differences in levels of meiotic transcription, which interferes with the formation of crossovers and thereby affects gBGC intensity within genes. Overall, the gBGC model explains 81.3% of the variance in SCU among genes. We argue that the strong heterogeneity of SCU induced by gBGC in mammalian genomes precludes any optimization of the tRNA pool to the demand in codon usage.

evolutionary biology↗

bioRxiv2016

Cladogenetic and Anagenetic Models of Chromosome Number Evolution: a Bayesian Model Averaging Approach

Chromosome number is a key feature of the higher-order organization of the genome, and changes in chromosome number play a fundamental role in evolution. Dysploid gains and losses in chromosome number, as well as polyploidization events, may drive reproductive isolation and lineage diversification. The recent development of probabilistic models of chromosome number evolution in the groundbreaking work by Mayrose et al. (2010, ChromEvol) have enabled the inference of ancestral chromosome numbers over molecular phylogenies and generated new interest in studying the role of chromosome changes in evolution. However, the ChromEvol approach assumes all changes occur anagenetically (along branches), and does not model events that are specifically cladogenetic. Cladogenetic changes may be expected if chromosome changes result in reproductive isolation. Here we present a new class of models of chromosome number evolution (called ChromoSSE) that incorporate both anagenetic and cladogenetic change. The ChromoSSE models allow us to determine the mode of chromosome number evolution; is chromosome evolution occurring primarily within lineages, primarily at lineage splitting, or in clade-specific combinations of both? Furthermore, we can estimate the location and timing of possible chromosome speciation events over the phylogeny. We implemented ChromoSSE in a Bayesian statistical framework, specifically in the software RevBayes, to accommodate uncertainty in parameter estimates while leveraging the full power of likelihood based methods. We tested ChromoSSEs accuracy with simulations and re-examined chromosomal evolution in Aristolochia, Carex section Spirostachyae, Helianthus, Mimulus sensu lato (s.l.), and Primula section Aleuritia, finding evidence for clade-specific combinations of anagenetic and cladogenetic dysploid and polyploid modes of chromosome evolution.

evolutionary biology↗

bioRxiv2016

Revisiting the effect of red on competition in humans

Bright red coloration is a signal of male competitive ability in animal species across a range of taxa, including non-human primates. Does the effect of red on competition extend to humans? A landmark study in evolutionary psychology established such an effect through analysis of data for four combat sports at the 2004 Athens Olympics [1]. Here we show that the results do not replicate in an equivalent, independent dataset for the 2008 Beijing Olympics, and that there is substantial variation in the fraction of wins by red across sports in both years. We uncover a number of shortcomings with the research design, analysis, and interpretation underlying the original results. For example, the variation observed in the data may reflect bias towards wins by one color over the other, linked to specific features of the tournament structure for the sports analysed. Reanalysis of the data to address these shortcomings indicates that there is no evidence for an effect of red on the outcomes of Olympic combat sports. Our results refute past claims based on analysis of this system, challenging the related notion that any effect of red in human competition is an evolved response shaped by sexual selection.

evolutionary biology↗