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bioRxiv2016

Can secondary contact following range expansion be distinguished from barriers to gene flow?

Secondary contact is the reestablishment of gene flow between sister populations that have diverged. For instance, at the end of the Quaternary glaciations in Europe, secondary contact occurred during the northward expansion of the populations which had found refugia in the southern peninsulas. With the advent of multi-locus markers, secondary contact can be investigated using various molecular signatures including gradients of allele frequency, admixture clines, and local increase of genetic differentiation. We use coalescent simulations to investigate if molecular data provide enough information to distinguish between secondary contact following range expansion and an alternative evolutionary scenario consisting of a barrier to gene flow in an isolation-by-distance model. We find that an excess of Linkage Disequilibrium and of genetic diversity at the suture zone is a unique signature of secondary contact. We also find that the directionality index {Psi}, which was proposed to study range expansion, is informative to distinguish between the two hypotheses. However, although evidence for secondary contact is usually conveyed by statistics related to admixture coefficients, we find that they can be confounded by isolation-by-distance. We recommend to account for the spatial repartition of individuals when investigating secondary contact in order to better reflect the complex spatio-temporal evolution of populations and species.

Evolutionary Biology↗

bioRxiv2016

Most Compositae (Asteraceae) are descendants of a paleohexaploid and all share a paleotetraploid ancestor with the Calyceraceae

Premise of the studyLike many other flowering plants, members of the Compositae (Asteraceae) have a polyploid ancestry. Previous analyses have found evidence for an ancient duplication or possibly triplication in the early evolutionary history of the family. We sought to better place this paleopolyploidy in the phylogeny and assess its nature.\n\nMethodsWe sequenced new transcriptomes for Barnadesia, the lineage sister to all other Compositae, and four representatives of closely related families. Using a recently developed algorithm, MAPS, we analyzed nuclear gene family phylogenies for evidence of paleopolyploidy.\n\nKey resultsWe found that the previously recognized Compositae paleopolyploidy is also in the ancestry of the Calyceraceae. Our phylogenomic analyses uncovered evidence for a successive second round of genome duplication among all sampled Compositae except Barnadesia.\n\nConclusionsOur analyses of new samples with new tools provide a revised view of paleopolyploidy in the Compositae. Together with results from recent linkage maps, our results suggest that the Compositae and Calyceraceae have a common paleotetraploid ancestor and most Compositae are descendants of a paleohexaploid. Although paleohexaploids have been previously identified, this is the first example where the paleotetraploid and paleohexaploid lineages have survived over tens of millions of years. The complex polyploidy in the ancestry of the Compositae and Calyceraceae represents a unique opportunity to study the long-term evolutionary fates and consequences of different ploidal levels.

Evolutionary Biology↗

bioRxiv2016

Royal decree: gene expression in transgenerationally immune primed bumblebee workers mimics a primary immune response

Invertebrates lack the cellular and physiological machinery of the adaptive immune system, but show specificity in their immune response [1, 2] and immune priming [3-11]. Functionally, immune priming is comparable to immune memory in vertebrates. Individuals that have survived exposure to a given parasite are better protected against subsequent exposures. Protection may be cross-reactive (e.g. [12]), but demonstrations of persistent and specific protection in invertebrates are increasing [3, 5]. This immune priming can cross generations (\"trans-generational\" immune priming) [4, 8], preparing offspring for the prevailing parasite environment. While these phenomena gain increasing support, the mechanistic foundations underlying such immune priming, both within and across generations, remain largely unknown. Using a transcriptomic approach, we show a bacterial challenge to bumblebee queens, known to induce trans-generational immune priming, alters daughter (worker) gene expression. Daughters, even when unchallenged themselves, constitutively express a core set of the genes induced upon direct bacterial exposure, including high expression of antimicrobial peptides, a beta-glucan receptor protein implicated in bacterial recognition and the induction of the toll signaling pathway[13], and slit-3 which is important in honeybee immunity[14]. Maternal challenge results in a distinct upregulation of their daughters immune system, with a signature overlapping with the induced individual response to a direct immune challenge. This will mediate mother-offspring protection, but also associated costs related to reconfiguration of constitutive immune expression. Identification of conserved immune pathways in memory-like responses has important implications for our understanding of the innate immune system, including the innate components in vertebrates, which share many of these pathways[15].\n\nAuthor SummaryInvertebrate individuals surviving exposure to an infectious disease can become better at fighting future infection by that same disease. This protection, known as immune priming, can even be transferred to the individuals offspring. The functional outcome is very similar to that of vertebrate immune memory, but the mechanisms of how invertebrates achieve immune priming within an individual or across generations remain enigmatic. We found that bumblebee daughters of mothers exposed to a simulated bacterial infection express strongly many of the genes that they would activate if they were themselves infected. Our results show how immune priming across generations might be produced in bumblebees. Many parts of the invertebrate immune system are shared with us, and thus our study also sheds a light on how diverse immune memory-like effects could be achieved.

Evolutionary Biology↗

bioRxiv2016

Spirals, Scalp Whorls and Skin Biomechanics: Nature’s Own Design For Expansion

This paper began as an exercise in curiosity - logarithmic spiral designs abound in nature -- in galaxies, flowers, pinecones and on human scalps as whorls. Why are humans the only primates to have whorls on the scalp? Is the formation of scalp whorls mechanical or genetic? A mechanical theory has long been postulated- the mechanical theory suggests that hair whorl patterning is determined by the tension on the epidermis during rapid expansion of the cranium while the hair follicle is growing downwards - however, this has never before been experimentally proven conclusively. We found, that under certain conditions, we were able to experimentally recreate spirals on the scalp to demonstrate that the basis of scalp whorls is indeed mechanical - and that logarithmic spirals are indeed natures own design for rapid expansion of organic tissues. Given our experiments only created whorls when certain conditions were satisfied (and not in others), they have given us great insight into the mechanical formation of skin whorls and the physiology of skin stretch. We believe that these findings will lead to many more advances in understanding skin dynamics and indeed the behavior of any living tissue when confronted by stretch. As a corollary, the application of the results of these studies have led us to the discovery of a new surgical technique for closure of scalp defects using the golden spiral pattern, and this will be the subject of a separate paper.

Evolutionary Biology↗

bioRxiv2016

The role of transposable elements for gene expression in Capsella hybrids and allopolyploids

The formation of an allopolyploid species involves the merger of two genomes with separate evolutionary histories. In allopolyploids, genes derived from one progenitor species are often expressed at higher levels than those from the other progenitor. It has been suggested that this could be due to differences in transposable element (TE) content among progenitors, as silencing of TEs can affect expression of nearby genes. Here, we examine the role of TEs for expression biases in the widespread allotetraploid Capsella bursa-pastoris and in diploid F1 hybrids generated by crossing Capsella orientalis and Capsella rubella, two close relatives of the progenitors of C. bursa-pastoris. As C. rubella harbors more TEs than C. orientalis, we expect C. orientalis alleles to be expressed at higher levels if TE content is key for expression biases. To test this hypothesis, we quantified expression biases at approximately 5800 genes in flower buds and leaves, while correcting for read mapping biases using genomic data. While three of four C. bursa-pastoris accessions exhibited a shift toward higher relative expression of C. orientalis alleles, the fourth C. bursa-pastoris accession had the opposite direction of expression bias, as did diploid F1 hybrids. Associations between TE polymorphism and expression bias were weak, and the effect of TEs on expression bias was small. These results suggest that differences in TE content alone cannot fully explain expression biases in these species. Future studies should investigate the role of differences in TE silencing efficacy, as well as a broader set of other factors. Our results are important for a more general understanding of the role of TEs for cis-regulatory evolution in plants.

Evolutionary Biology↗

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↗