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Results for “Evolutionary Biology”

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bioRxiv2016

Genomic and Metagenomic Analyses Reveal Parallel Ecological Divergence in Heliosperma pusillum (Caryophyllaceae)

Cases of parallel ecological divergence in closely related taxa offer an invaluable material to study the processes of ecological speciation. Applying a combination of population genetic and metagenomic tools on a high-coverage RAD sequencing dataset, we test for parallel evolution across six population pairs of Heliosperma pusillum and H. veselskyi (Caryophyllaceae), two plant species found in the south-eastern Alps and characterized by clear morphological (glabrous vs. hairy) and ecological (alpine vs. montane, wet vs. dry) differentiation. Our analyses support a scenario of multiple independent instances of divergence between these species during the last 10,000 years. Structure analyses and simulations show that interspecific gene flow in each population pair is very low. A single locus, annotated as E3 ubiquitin ligase, an enzyme involved in plant innate immunity, shows a pattern of non-random segregation across populations of both species. A metagenomic analysis revealed information about contaminant exogenous DNA present in RAD sequencing libraries obtained from leaf material. Results of this analysis show clearly divergent bacterial and fungal phyllosphere communities between the species, but consistent communities across populations within each species. A similar set of biotic interactions is involved, together with abiotic factors, in shaping common selective regimes at different growing sites of each species. Different occurrences of H. veselskyi appear now genetically isolated from H. pusillum and from each other, and may independently proceed along the speciation continuum. Our work supports the hypothesis that repeated ecological divergence, observed here at an early stage, may be a common process of species diversification.

Evolutionary Biology↗

bioRxiv2016

Cis-regulatory evolution in prokaryotes revealed by interspecific archaeal hybrids.

The study of allele-specific expression (ASE) in interspecific hybrids has played a central role in our understanding of a wide range of phenomena, including genomic imprinting, X-chromosome inactivation, and cis-regulatory evolution. However across the hundreds of studies of hybrid ASE, all have been restricted to sexually reproducing eukaryotes, leaving a major gap in our understanding of the genomic patterns of cis-regulatory evolution in prokaryotes. Here we introduce a method to generate stable hybrids between two species of halophilic archaea, and measure genome-wide ASE in these hybrids with RNA-seq. We found that over half of all genes have significant ASE, and that genes encoding kinases show evidence of lineage-specific selection on their cis-regulation. This pattern of polygenic selection suggested species-specific adaptation to low phosphate conditions, which we confirmed with growth experiments. Altogether, our work extends the study of ASE to archaea, and suggests that cis-regulation can evolve under polygenic lineage-specific selection in prokaryotes.

Evolutionary Biology↗

bioRxiv2016

Adaptive divergence in transcriptome response to heat and acclimation in Arabidopsis thaliana plants from contrasting climates.

Phenotypic variation in stress response has been widely observed within species. This variation is an adaptive response to local climates and is controlled by gene sequence variation and especially by variation in expression at the transcriptome level. Plants from contrasting climates are thus expected to have different patterns in gene expression. Acclimation, a pre-exposure to sub-lethal temperature before exposing to extreme high temperature, is an important adaptive mechanism of plant survival. We are interested to evaluate the gene expression difference to heat stress for plants from contrasting climates and the role of acclimation in altering their gene expression pattern. Natural Arabidopsis thaliana plants from low elevation mediterranean and high elevation montane climates were exposed to two heat treatments at the bolting stage: a) 45{degrees}C: a direct exposure to 45{degrees}C heat; b) 38/45{degrees}C: an exposure to 45{degrees}C heat after a 38{degrees}C acclimation treatment. Variation in overall gene expression patterns was investigated. We also explored gene expression patterns for Hsp/Hsf pathway and reactive oxygen species (ROS) pathway. In both heat treatments, high elevation plants had more differentially expressed (DE) genes than low elevation plants. In 45{degrees}C, only Hsp/Hsf pathway was activated in low elevation plants; both Hsp/Hsf and ROS pathways were activated in high elevation plants. Small Hsps had the highest magnitude of change in low elevation plants while Hsp70 and Hsp90 showed the largest magnitude of fold in high elevation plants. In 38/45{degrees}C, Hsp/Hsf and ROS pathways were activated in both low and high elevation plants. Low elevation plants showed up-regulation in all Hsps, especially small Hsps; high elevation plants showed down-regulation in all Hsps. Low elevation and high elevation also adopted different genes in the ROS pathway. We also observed genes that shifted expression in both low and high elevation plants but with opposite directions of change. This study indicates that low and high elevation plants have evolved adaptive divergence in heat stress response. The contrasting patterns of temperature variation in low and high elevation sites appears to have played a strong role in the evolution of divergent patterns to high temperature stress, both pre-acclimation and direct exposure gene expression responses.\n\nMolecular EcologyThe Plant Journal IF: 6.8 (TPJ welcomes functional genomics manuscripts when a scientific question, rather than the technology used, has driven the research)

Evolutionary Biology↗

bioRxiv2016

Understanding Wolbachia acquisition and co-divergence of hosts and their associated bacteria: Wolbachia infection in the Chorthippus parallelus hybrid zone

Wolbachia is one of the best known bacterial endosymbionts affecting insects and nematodes. It is estimated that it infects 40% of insect species, so epidemiologically it may be considered a pandemic species. However, the mechanisms by which it is acquired from other species (horizontal transmission) or by which it coevolves with its hosts as a result of vertical transmission across generations are not known in detail. In fact, there are few systems in which the codivergence between host and bacterium has been described.\n\nThis study goes in deep in the Wolbachia infection in the grasshopper Chorthippus parallelus. This well-known system allows us to investigate the mechanism of acquisition of various Wolbachia strains in a new host, and the bacterial genomic changes during bacterial-host codivergence: We describe the genetic diversity of Wolbachia strains infecting both subspecies of C. parallelus and analyse their phylogenetic relationship. We also show the emergence of new bacterial alleles resulting from recombination events in Wolbachia infecting hybrid hosts. Our data suggest that F strains detected in this grasshopper have co-diverged with its host, versus a more recent horizontal transmission of B strains. According with this, we discuss the potential role of Wolbachia in the dynamics of the grasshopper hybrid zone and in the divergence of the two grasshopper subspecies since the origin of their hybrid zone.

Evolutionary Biology↗

bioRxiv2016

In-vivo mutation rates and fitness landscape of HIV-1

Mutation rates and fitness costs of deleterious mutations are difficult to measure in vivo but essential for a quantitative understanding of evolution. Using whole genome deep sequencing data from longitudinal samples during untreated HIV-1 infection, we estimated mutation rates and fitness costs in HIV-1 from the temporal dynamics of genetic variation. At approximately neutral sites, mutations accumulate with a rate of 1.2 x 10-5 per site per day, in agreement with the rate measured in cell cultures. The rate from G to A is largest, followed by the other transitions C to T, T to C, and A to G, while transversions are more rare. At non-neutral sites, most mutations reduce virus replication; using a model of mutation selection balance, we estimated the fitness cost of mutations at every site in the HIV-1 genome. About half of all nonsynonymous mutations have large fitness costs (greater than 10%), while most synonymous mutations have costs below 1%. The cost of synonymous mutations is especially low in most of gag and pol, while much higher costs are observed in important RNA structures and regulatory regions. The intrapatient fitness cost estimates are consistent across multiple patients, suggesting that the deleterious part of the fitness landscape is universal and explains a large fraction of global HIV-1 group M diversity.

Evolutionary Biology↗

bioRxiv2016

Genome sequence of tsetse bracoviruses: insights into symbiotic virus evolution

Mutualism between endogenous viruses and eukaryotes is still poorly understood. Whole genome data has highlighted the diverse distribution of viral sequences in several eukaryote host genomes. A group of endogenous double-stranded polydnaviruses known as bracoviruses has been identified in parasitic braconid wasp (Hymenoptera). Bracoviruses allow wasps to reproductively co-opt other insect larvae. Bracoviruses are excised from the host genome and injected in to the larva along side the wasp eggs; where they encode proteins that lower host immunity allowing development of parasitoid wasp larvae in the host. Interestingly, putative bracoviral sequences have recently been detected in the first sequenced genome of the tsetse fly (Diptera). This is peculiar since tsetse flies do not share this reproductive lifestyle. To investigate genome rearrangements associated with these unique mutual symbiotic relationships and examine its value as a potential vector control strategy entry point. We use comparative genomics to determine the presence, prevalence and genetic diversity of bracoviruses of five tsetse fly species (G. austeni, G. brevipalpis, G. f. fuscipes, G. m. morsitans and G. pallidipes) and the housefly (Musca domestica). We identify and use four viral Maverick genes as evolutionary models for bracoviruses. This is the first record of homologous bracoviruses in multiple Dipteran genomes. Phylogenetic reconstruction of each gene revealed two major clades that represent the two types of Mavericks. We detect varying magnitudes of purifying selection across these loci except for the poxvirus A32 gene, which is under positive selection. Moreover, these genes were inserted at conserved regions and co-evolve at similar rates with the host genomes.

Evolutionary Biology↗

bioRxiv2016

Adaptation in protein fitness landscapes is facilitated by indirect paths

The structure of fitness landscapes is critical for understanding adaptive protein evolution (e.g. antimicrobial resistance, affinity maturation, etc.). Due to limited throughput in fitness measurements, previous empirical studies on fitness landscapes were confined to either the neighborhood around the wild type sequence, involving mostly single and double mutants, or a combinatorially complete subgraph involving only two amino acids at each site. In reality, however, the dimensionality of protein sequence space is higher (20L, L being the length of the relevant sequence) and there may be higher-order interactions among more than two sites. To study how these features impact the course of protein evolution, we experimentally characterized the fitness landscape of four sites in the IgG-binding domain of protein G, containing 204 = 160,000 variants. We found that the fitness landscape was rugged and direct paths of adaptation were often constrained by pairwise epistasis. However, while direct paths were blocked by reciprocal sign epistasis, we found systematic evidence that such evolutionary traps could be circumvented by \"extra-dimensional bypass\". Extra dimensions in sequence space - with a different amino acid at the site of interest or an additional interacting site - open up indirect paths of adaptation via gain and subsequent loss of mutations. These indirect paths alleviate the constraint on reaching high fitness genotypes via selectively accessible trajectories, suggesting that the heretofore neglected dimensions of sequence space may completely change our views on how proteins evolve.

Evolutionary Biology↗

bioRxiv2016

Phylogenetic expression profiling reveals widespread coordinated evolution of gene expression

Phylogenetic profiling, which infers functional relationships between genes based on patterns of gene presence/absence across species, has proven to be highly effective. Here we introduce a complementary approach, phylogenetic expression profiling (PEP), which detects gene sets with correlated expression levels across a phylogeny. Applying PEP to RNA-seq data consisting of 657 samples from 309 diverse unicellular eukaryotes, we found several hundred gene sets evolving in a coordinated fashion. These allowed us to predict a role of the Golgi apparatus in Alzheimer's disease, as well as novel genes related to diabetes pathways. We also detected adaptive evolution of tRNA ligase levels to match genome-wide codon usage. In sum, we found that PEP is an effective method for inferring functional relationships - especially among core cellular components that are never lost, to which phylogenetic profiling cannot be applied - and that many subunits of the most conserved molecular machines are coexpressed across eukaryotes.

Evolutionary Biology↗

bioRxiv2016

Signatures of archaic adaptive introgression in present-day human populations

Comparisons of DNA from archaic and modern humans show that these groups interbred, and in some cases received an evolutionary advantage from doing so. This process - adaptive introgression - may lead to a faster rate of adaptation than is predicted from models with mutation and selection alone. Within the last couple of years, a series of studies have identified regions of the genome that are likely examples of adaptive introgression. In many cases, once a region was ascertained as being introgressed, commonly used statistics based on both haplotype as well as allele frequency information were employed to test for positive selection. Introgression by itself, however, changes both the haplotype structure and the distribution of allele frequencies, thus confounding traditional tests for detecting positive selection. Therefore, patterns generated by introgression alone may lead to false inferences of positive selection. Here we explore models involving both introgression and positive selection to investigate the behavior of various statistics under adaptive introgression. In particular, we find that the number and allelic frequencies of sites that are uniquely shared between archaic humans and specific present-day populations are particularly useful for detecting adaptive introgression. We then examine the 1000 Genomes dataset to characterize the landscape of uniquely shared archaic alleles in human populations. Finally, we identify regions that were likely subject to adaptive introgression and discuss some of the most promising candidate genes located in these regions.

Evolutionary Biology↗

bioRxiv2016

Escherichia coli populations adapt to complex, unpredictable fluctuations without any trade-offs across environments

In nature, organisms are simultaneously exposed to multiple stresses (i.e. complex environments) that often fluctuate unpredictably. While both these factors have been studied in isolation, the interaction of the two remains poorly explored. To address this issue, we selected laboratory populations of Escherichia coli under complex (i.e. stressful combinations of pH, H2O2 and NaCl) unpredictably fluctuating environments for ~900 generations. We compared the growth rates and the corresponding trade-off patterns of these populations to those that were selected under constant values of the component stresses (i.e. pH, H2O2 and NaCl) for the same duration. The fluctuation-selected populations had greater mean growth rate and lower variation for growth rate over all the selection environments experienced. However, while the populations selected under constant stresses experienced severe tradeoffs in many of the environments other than those in which they were selected, the fluctuation-selected populations could by-pass the across-environment trade-offs completely. Interestingly, trade-offs were found between growth rates and carrying capacities. The results suggest that complexity and fluctuations can strongly affect the underlying trade-off structure in evolving populations.

Evolutionary Biology↗

bioRxiv2016

Genomic evidence for population-specific responses to coevolving parasites in a New Zealand freshwater snail

Reciprocal coevolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population- or genotype-specific evolutionary change. These host-parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of coevolving host-parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its coevolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus-infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population-level coevolution is leading to population-specific host-parasite interactions and evolutionary trajectories. We also used an FST-based approach to identify a set of loci that represent promising candidates for targets of parasite-mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population-specific responses to coevolving infection in the P. antipodarum-Microphallus interaction and provide new insights into the genomic basis of coevolutionary interactions in nature.

Evolutionary Biology↗

bioRxiv2016

Experimental evidence for sexual selection against inbred males when it truly counts

Although there are many correlational studies, unbiased estimates of inbreeding depression only come from experimental studies that create inbred and outbred individuals. Few such studies determine the extent to which inbreeding depression in males is due to natural or sexual selection. Importantly, traits that are closely related to fitness are predicted to be most strongly affected by inbreeding depression, so measuring fitness or key fitness components, rather than phenotypic traits, is necessary to estimate inbreeding depression accurately. Here, we experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki) by mating full-sibs (f=0.25). We show this led to a 23% reduction in genome-wide heterozygosity. Males were then raised on different diets early in life. We then allowed adult males to compete freely for females to test if inbreeding, early diet, and their interaction affect a males share of paternity. Early diet had no effect on paternity, but outbred males sired almost twice as many offspring as inbred males. We also found that males with a relatively long gonopodium (intromittent organ) had greater reproductive success. We demonstrate that inbreeding has important consequences because it negatively affects a key component of male fitness. Given there was no difference in adult mortality this finding can only be due to inbreeding negatively affecting sexually selected traits.

Evolutionary Biology↗

bioRxiv2016

Sexual selection on body size, genitals and heterozygosity: effects of demography and habitat complexity

Environmental variation can maintain genetic variation in sexually selected traits if it affects the strength of directional selection. Specifically, environmental variation in sex-specific mortality will change the operational sex ratio (OSR), which predicts the intensity of mating competition. How the OSR affects selection for specific male traits is poorly understood; and it is unknown how often sexual selection is affected by interactions between the OSR and environmental factors that alter social variables such as mate encounter rates. Here, we experimentally manipulated the OSR and habitat complexity and quantified sexual selection on male mosquitofish (Gambusia holbrooki). In G. holbrooki there is high within-population variation in male size, which may exist because of a tradeoff between the ability to sneak copulate (favouring small males) and monopolize females (favouring large males). The success of each tactic is predicted to depend on the OSR, encounter rates and the ability to stealthily approach conspecifics. We show that, despite greater sharing of paternity under a male-biased OSR, neither the opportunity for selection, nor selection on male traits was affected by the OSR or habitat complexity. Instead, sexual selection consistently favored smaller males with high genetic heterozygosity (using >3000 SNP markers), and a relatively long gonopodium (intromittent organ).

Evolutionary Biology↗

bioRxiv2016

Evolutionary stability of microbial communities with antibiotic degrading species

A major puzzle in ecology is how antibiotic resistant, sensitive and producer species coexist in close proximity. Recently, we showed that antibiotic degrading species dramatically alter community dynamics: replacing intrinsic resistance with resistance through degradation generates stable communities resilient to spatial mixing, large species abundance perturbations, changes in interaction strengths, and differences in species growth rates. In addition to ecological stability, it is interesting to consider evolutionary stability of these communities to the appearance of cheater species that either cease production or degradation of antibiotics. Our investigation of evolutionary stability of cyclical 3-species communities revealed that these communities are robust to cheaters that stop degrading antibiotics. Our simulations also showed that cheaters that stop producing antibiotics do not take over the community, yet they can transiently invade and cause community collapse. In the analytical approximation we initially investigated, production cheaters with a small fitness advantage can invade the community simply because the benefit of inhibiting competitors is shared among all cells. Here, we consider evolutionary stability to cheaters in our complete model, where spatial mixing is introduced only after a short range colonization step. In this regime, an antibiotic producer cell directly benefits from killing nearby competitor species as it has a greater chance of colonizing the newly voided spaces created by the action of its antibiotic. Simulating response to cheater invasions for the cyclical three species community and for random 4-species ecologically stable topologies, we find that these communities can be fully resilient to both degradation and production cheaters. The strength of selection against cheaters varies with the area of the zone of inhibition around producers and is maximized for weak inhibition, where there is less overlap between the killing zones of neighboring cells. These results may aid the construction of complex synthetic communities that are both ecological and evolutionary stable.

Evolutionary Biology↗

bioRxiv2016

Are sexually selected traits affected by a poor environment early in life?

Conditions experienced early in life can affect key life-history traits. Individuals that experience a poor nutritional environment early in life can reduce potential costs by delaying sexual maturation. The direct costs of delaying maturation are well known (i.e. delayed onset of breeding), but individuals can also face additional costs as adults. Some of these hidden costs accrue due to cryptic morphological and physiological changes. In mosquitofish (Gambusia holbrooki), males with limited food intake early in life delay maturation to eventually reach a similar adult body size to their well-fed counterparts ( catch-up growth). Here we tested whether a poor diet early in life incurs hidden costs due to reduced expression of sexually selected male traits (genital size and ejaculate traits). We found that diet early in life significantly influenced sperm reserves and replenishment rate due to age and development-rate dependent effects. Although catching-up in body size ameliorates some of the costs of a poor start in life for males, our findings suggest that long-term fitness costs might arise because of sexually selection against these males. Our results highlight that fitness costs of a poor start in life can extend into adulthood.

Evolutionary Biology↗

bioRxiv2016

Mixing of Porpoise Ecotypes in South Western UK Waters Revealed by Genetic Profiling

Contact zones between marine ecotypes are of interest for understanding how key pelagic predators may react to climate change. We analysed the fine scale genetic structure and morphological variation in harbour porpoises around the UK, at the proposed northern limit of a contact zone between southern and northern ecotypes in the Bay of Biscay. Using a sample of 591 stranded animals spanning a decade and microsatellite profiling at 9 loci, clustering and spatial analyses revealed that animals stranded around UK are composed of mixed genetic ancestries from two genetic pools. Porpoises from SW England displayed a distinct genetic ancestry, had larger body-sizes and inhabit an environment differentiated from other UK costal areas. Genetic ancestry blends from one group to the other along a SW-NE axis along the UK coastline, and showed a significant association with body size, consistent with morphological differences between the two ecotypes and their mixing around the SW coast. We also found significant isolation-by-distance among juveniles, suggesting that stranded juveniles display reduced intergenerational dispersal, while adults show larger variance. The fine scale structure of this admixture zone raises the question of how it will respond to future climate change and provides a reference point for further study.

Evolutionary Biology↗

bioRxiv2016

Evolutionary determinants of morphological polymorphism in colonial animals

Colonial animals commonly exhibit morphologically polymorphic modular units that are phenotypically distinct and specialize in specific functional tasks. But how and why these polymorphic modules have evolved is poorly understood. Across colonial invertebrates there is wide variation in the degree of polymorphism from none in colonial ascidians, to extreme polymorphism in siphonophores such as the Portuguese Man of War. Bryozoa are a phylum of exclusively colonial invertebrates that uniquely exhibit almost the entire range of polymorphism from monomorphic species to others that rival siphonophores in their polymorphic complexity. Previous approaches to understanding the evolution of polymorphism have been based upon analyses of (1) the functional role of polymorphs or (2) presumed evolutionary costs and benefits based upon evolutionary theory that postulates polymorphism should only be evolutionarily sustainable in more \"stable\" environments because polymorphism commonly leads to the loss of feeding and sexual competence. Here we use bryozoans from opposite shores of the Isthmus of Panama to revisit the environmental hypothesis by comparison of faunas from distinct oceanographic provinces that differ greatly in environmental variability and we then examine the correlations between the extent of polymorphism in relation to patterns of ecological succession and variation in life histories. We find no support for the environmental hypothesis. Distributions of the incidence of polymorphism in the oceanographically unstable Eastern Pacific are indistinguishable from those in the more stable Caribbean. In contrast, the temporal position of species in a successional sequence is collinear with the degree of polymorphism because species with fewer types of polymorphs are competitively replaced by species with higher numbers of polymorphs on the same substrata. Competitively dominant species also exhibit patterns of growth that increase their competitive ability. The association between degrees of polymorphism and variations in life histories is fundamental to understanding of the macroevolution of polymorphism.

Evolutionary Biology↗

bioRxiv2016

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization in Drosophila

Argonaute2 (Ago2) is a rapidly evolving nuclease in the Drosophila melanogaster RNA interference (RNAi) pathway that targets viruses and transposable elements in somatic tissues. Here we reconstruct the history of Ago2 duplications across the Drosophila obscura group, and use patterns of gene expression to infer new functional specialization. We show that some duplications are old, shared by the entire species group, and that losses may be common, including previously undetected losses in the lineage leading to D. pseudoobscura. We find that while the original (syntenic) gene copy has generally retained the ancestral ubiquitous expression pattern, most of the novel Ago2 paralogues have independently specialized to testis-specific expression. Using population genetic analyses, we show that most testis-specific paralogues have significantly lower genetic diversity than the genome-wide average. This suggests recent positive selection in three different species, and model-based analyses provide strong evidence of recent hard selective sweeps in or near four of the six D. pseudoobscura Ago2 paralogues. We speculate that the repeated evolution of testis-specificity in obscura group Ago2 genes, combined with their dynamic turnover and strong signatures of adaptive evolution, may be associated with highly derived roles in the suppression of transposable elements or meiotic drive. Our study highlights the lability of RNAi pathways, even within well-studied groups such as Drosophila, and suggests that strong selection may act quickly after duplication in RNAi pathways, potentially giving rise to new and unknown RNAi functions in non-model species.\n\nSupporting DataAll new sequences produced in this study have been submitted to Genbank as KX016642-KX016771.

Evolutionary Biology↗