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bioRxiv2018

The evolution, distribution and diversity of endogenous circoviral elements

Circoviruses (family Circoviridae) are small, non-enveloped viruses that have short, single-stranded DNA genomes. Circovirus sequences are frequently recovered in metagenomic investigations, indicating that these viruses are widespread, yet they remain relatively poorly understood. Endogenous circoviral elements (CVe) are DNA sequences derived from circoviruses that occur in vertebrate genomes. CVe can provide unique, retrospective information about the biology and evolution of circoviruses. In this study, we screened 362 vertebrate genome assemblies in silico to generate a catalog of CVe loci. We identified a total of 179 CVe sequences, most of which have not been reported previously. We show that these CVe loci reflect at least 19 distinct germline integration events. We determine the structure of CVe loci, identifying some that show evidence of potential functionalization. We also identify orthologous copies of CVe in snakes, fish, birds, and mammals, allowing us to add new calibrations to the timeline of circovirus evolution. Finally, we observed that some ancient CVe group robustly with contemporary circoviruses in phylogenies, with all sequences within these groups being derived from the same host class or order, implying a hitherto underappreciated stability in circovirus-host relationships. The openly available dataset constructed in this investigation provides new insights into circovirus evolution, and can be used to facilitate further studies of circoviruses and CVe.\n\nAbbreviations

evolutionary biology↗

bioRxiv2018

Tradeoffs and cultural diversity

Culture is humanitys prime adaptation. Which cultural traits contribute to adaptive value at the level of cultural groups, and how they do so, is, however, unclear and debated. Here, we apply an approach from systems biology, known as Pareto task inference (ParTI), to bring a fresh perspective to these questions. ParTI considers systems that need to perform multiple tasks. No system can be optimal at all tasks at once, leading to a fundamental tradeoff. These tradeoffs result in specific patterns in multivariate trait data: data falls inside polygons in trait space, whose vertices are trait combinations that are adaptive for each of the tasks. ParTI can infer the number of adaptive tasks and their nature without need for a-priori assumptions, based on the vertices of these polygons. Here, we applied ParTI to two datasets of cultural traits, on Austronesian cultures and modern hunter-gatherers, adjusting for phylogeny and spatial diffusion effects. We find evidence that these independent datasets show a tradeoff between the same three tasks. We identify the tasks as resource defense, resource competition, and mobility/exchange. Specific combinations of cultural traits are adaptive for each of these tasks. This approach can be widely applied to any large multivariate dataset to study trade-offs in cultural evolution.

evolutionary biology↗

bioRxiv2017

Ancient duplication and horizontal transfer of a toxin gene cluster reveals novel mechanisms in the cercosporin biosynthesis pathway

Species in the genus Cercospora cause economically devastating diseases in sugar beet, maize, rice, soy bean and other major food crops. Here we sequenced the genome of the sugar beet pathogen C. beticola and found it encodes 63 putative secondary metabolite gene clusters, including the cercosporin toxin biosynthesis (CTB) cluster. We show that the CTB gene cluster has experienced multiple duplications and horizontal transfers across a spectrum of plant pathogenic fungi, including the wide host range Colletotrichum genus as well as the rice pathogen Magnaporthe oryzae. Although cercosporin biosynthesis has been thought to-date to rely on an eight gene CTB cluster, our phylogenomic analysis revealed gene collinearity adjacent to the established cluster in all CTB cluster-harboring species. We demonstrate that the CTB cluster is larger than previously recognized and includes cercosporin facilitator protein (CFP) previously shown to be involved with cercosporin auto-resistance, and four additional genes required for cercosporin biosynthesis including the final pathway enzymes that install the unusual cercosporin methylenedioxy bridge. Finally, we demonstrate production of cercosporin by Colletotrichum fioriniae, the first known cercosporin producer within this agriculturally important genus. Thus, our results provide new insight into the intricate evolution and biology of a toxin critical to agriculture and broaden the production of cercosporin to another fungal genus containing many plant pathogens of important crops worldwide.\n\nSignificance StatementSpecies in the fungal genus Cercospora cause diseases in many important crops worldwide. Their success as pathogens is largely due to the secretion of cercosporin during infection. We report that the cercosporin toxin biosynthesis (CTB) cluster is ancient and was horizontally transferred to diverse fungal pathogens on an unprecedented scale. Since these analyses revealed genes adjacent to the established CTB cluster, we evaluated their role in C. beticola to show that four are necessary for cercosporin biosynthesis. Finally, we confirmed that the apple pathogen Colletotrichum fioriniae produces cercosporin, the first case outside the family Mycosphaerellaceae. Other Colletotrichum plant pathogens also harbor the CTB cluster, which points to a wider concern that this toxin may play in virulence and human health.

evolutionary biology↗

bioRxiv2014

Sensitivity of quantitative traits to mutational effects, number of loci, and population history

When models of quantitative genetic variation are built from population genetic first principles, several assumptions are often made. One of the most important assumptions is that traits are controlled by many genes of small effect. This leads to a prediction of a Gaussian trait distribution in the population, via the Central Limit Theorem. Since these biological assumptions are often unknown or untrue, we characterized how finite numbers of loci or large mutational effects can impact the sampling distribution of a quantitative trait. To do so, we developed a neutral coalescent-based framework, allowing us to experiment freely with the number of loci and the underlying mutational model. Through both analytical theory and simulation we found the normality assumption was highly sensitive to the details of the mutational process, with the greatest discrepancies arising when the number of loci was small or the mutational kernel was heavy-tailed. In particular, fat-tailed mutational kernels result in multimodal sampling distributions for any number of loci. An empirical analysis of 7079 expressed genes in 49 Neurospora crassa strains identified 116 genes with non-normal sampling distributions. Several genes showed evidence of multimodality and/or skewness, suggesting the importance of their genetic architecture. Since selection models and robust neutral models may produce qualitatively similar sampling distributions, we advise extra caution should be taken when interpreting model-based results for poorly understood systems of quantitative traits.

Evolutionary Biology↗

bioRxiv2018

Heritability, selection, and the response to selection in the presence of phenotypic measurement error: effects, cures, and the role of repeated measurements

Quantitative genetic analyses require extensive measurements of phenotypic traits, a task that is often not trivial, especially in wild populations. On top of instrumental measurement error, some traits may undergo transient (i.e. non-persistent) fluctuations that are biologically irrelevant for selection processes. These two sources of variability, which we denote here as measurement error in a broad sense, are possible causes for bias in the estimation of quantitative genetic parameters. We illustrate how in a continuous trait transient effects with a classical measurement error structure may bias estimates of heritability, selection gradients, and the predicted response to selection. We propose strategies to obtain unbiased estimates with the help of repeated measurements taken at an appropriate temporal scale. However, the fact that in quantitative genetic analyses repeated measurements are also used to isolate permanent environmental instead of transient effects, requires a re-assessment of the information content of repeated measurements. To do so, we propose to distinguish \"short-term\" from \"long-term\" repeats, where the former capture transient variability and the latter the permanent effects. We show how the inclusion of the corresponding variance components in quantitative genetic models yields unbiased estimates of all quantities of interest, and we illustrate the application of the method to data from a Swiss snow vole population.

evolutionary biology↗

bioRxiv2017

Ancestral Reconstruction of Gene Blocks using an Event-Based Method

Complexity is a fundamental attribute of life. Complex systems are made of parts that together perform functions that a single component, or subsets containing individual components, cannot. Examples of complex molecular systems include protein structures such as the F1Fo-ATPase, the ribosome, or the flagellar motor: each one of these structures requires most or all of its components to function properly. Given the ubiquity of complex systems in the biosphere, understanding the evolution of complexity is central to biology. At the molecular level, operons are a classic example of a complex system. An operons genes are co-transcribed under the control of a single promoter to a polycistronic mRNA molecule, and the operons gene products often form molecular complexes or metabolic pathways. With the large number of complete bacterial genomes available, we now have the opportunity to explore the evolution of these complex entities, by identifying possible intermediate states of operons. In this work, we developed a maximum parsimony algorithm to reconstruct ancestral operon states, and show a simple vertical evolution model of how operons may evolve from the individual component genes. We describe several ancestral states that are plausible functional intermediate forms leading to the full operon. We also offer Reconstruction of Ancestral Gene blocks Using Events or ROAGUE as a software tool for those interested in exploring gene block and operon evolution.\n\nThe software accompanying this paper is available under GPLv3 license in: https://github.com/nguyenngochuy91/Ancestral-Blocks-Reconstruction.\n\nAll figures in this paper are available in enlarged downloadable form from:https://github.com/nguyenngochuy91/Ancestral-Blocks-Reconstruction/tree/master/images

evolutionary biology↗

bioRxiv2017

The development of scientific consensus: analyzing conflict and concordance among Avian phylogenies

Recent developments in phylogenetic methods and data acquisition have allowed for the construction of large and comprehensive phylogenetic relationships. Published phylogenies represent an enormous resource that not only facilitate the resolution of questions related to comparative biology, but also provide a resource on which to gauge the development of consensus across the tree of life. From the Open Tree of Life, we gathered 290 avian phylogenies representing all major groups that have been published over the last few decades and analyzed how concordance and conflict develop among these trees through time. Nine large scale backbone trees (including a new synthetic tree from this study) were used for the consensus assessment. We found that conflicts were over-represented both along the backbone (higher-level neoavian relationships) and within the oscine Passeriformes. Importantly, although we have made major strides in our knowledge of major clades, recent published comprehensive trees, as well as trees of individual clades, continue to contribute significantly to the resolution of clades in the avian phylogeny. These findings are somewhat unexpected, given that birds constitute a relatively well-studied and small clade of the tree of life (i.e., Aves). Therefore, our analysis highlights that much work is still needed before we can confidently resolve the less well studied areas of the tree of life.

evolutionary biology↗

bioRxiv2017

Population Genomics of the Foothill Yellow-Legged Frog (Rana boylii) and RADseq Parameter Choice for Large-Genome Organisms

Genomic data are useful for attaining high resolution in population genetic studies and have become increasingly available for answering questions in biological conservation. We analyzed RADseq data for the protected foothill yellow-legged frog (Rana boylii) throughout its native range in California and Oregon, including many of the same localities included in an earlier study based on mitochondrial DNA. We recovered five primary clades that correspond to geographic regions within California and Oregon, with better resolution and more spatially consistent patterns than the previous study, confirming the increased resolving power of genomic approaches compared to single-locus analyses. Bayesian clustering, PCA and population differentiation with admixture analyses all indicated that approximately half the range of R. boylii consists of a single, relatively uniform population, while regions in the Sierra Nevada and Central Coast Range of California are deeply differentiated genetically. Additionally, a major methodological challenge for large genome organisms, including many amphibians, is deciding on sequence similarity clustering thresholds for population genetic analyses using RADseq data, and we develop a novel set of metrics that allow researchers to set a sequence similarity threshold that maximizes the separation of paralogous regions while minimizing the oversplitting of naturally occurring allelic variation within loci.

evolutionary biology↗

bioRxiv2018

Multiple independent adaptations to different ranges of host plants indicate high adaptability despite clonal reproduction in the nematode pest Meloidogyne incognita

The most devastating nematodes to worldwide agriculture are the root-knot nematodes with Meloidogyne incognita being the most widely distributed and damaging species. This parasitic and ecological success seem surprising given its supposed obligatory clonal reproduction. Clonal reproduction has been suspected based on cytological observations but, so far, never confirmed by population genomics data. At the species level, M. incognita is highly polyphagous with thousands of host plants. However, the host range varies among different M. incognita isolates that may present distinct and more restricted host compatibilities. Historically, four host races had been defined as a function of ranges of compatible and incompatible plants. We sequenced the genomes of 11 isolates across Brazil, covering these four distinct races to assess (i) how clonal reproduction is and (ii) how the level of genome variability associates with biological traits such as the host races, affected agronomic culture, and geographical distribution. By aligning the genomic reads of the isolates to the M. incognita reference genome assembly, we identified SNV and small-scale insertions/deletions. Analysis of linkage disequilibrium and 4-gametes test, showed no sign of recombination, confirming the clonal mode of reproduction of M. incognita. We showed that there are relatively few point variations between the different isolates, and these variations show no significant association with either the host races, the geographical origin of the samples or the host plant on which they have been collected. Due to the lack of phylogenetic signal underlying their existence, we recommend the discontinuation of the terminology race. Overall, these results suggest that multiple gains and losses of parasitic abilities and adaptations to different environmental conditions account for the broad host spectrum and wide geographic distribution of M. incognita. Hence, this nematode constitutes a model species to study adaptability without sexual recombination and overall low genomic variations in animals.

evolutionary biology↗

bioRxiv2018

Expansion of the fatty acyl reductase gene family shaped pheromone communication in Hymenoptera

The conserved fatty acyl reductase (FAR) family is involved in biosynthesis of fatty alcohols that serve a range of biological roles. In moths, butterflies (Lepidoptera), and bees (Hymenoptera), FARs biosynthesize fatty alcohol pheromones participating in mate-finding strategies. Using a combination of next-generation sequencing, analysis of transposable elements (TE) in the genomic environment of FAR genes, and functional characterization of FARs from Bombus lucorum, B. lapidarius, and B. terrestris, we uncovered a massive expansion of the FAR gene family in Hymenoptera, presumably facilitated by TEs. Expansion occurred in the common ancestor of bumblebees (Bombini) and stingless bees (Meliponini) after their divergence from the honeybee lineage. We found that FARs from the expanded FAR-A orthology group contributed to the species-specific male marking pheromone composition. Our results indicate that TE-mediated expansion and functional diversification of the FAR gene family played a key role in the evolution of pheromone communication in the crown group of Hymenoptera.\n\nAbbreviationsMMP: male marking pheromone, FA: fatty acid, FAME: fatty acid methyl ester, FAR: fatty acyl reductase, LG: labial gland, FB: fat body, TE: transposable element.

evolutionary biology↗

bioRxiv2016

Cytoplasmic-nuclear incompatibility between wild-isolates of Caenorhabditis nouraguensis

How species arise is a fundamental question in biology. Species can be defined as populations of interbreeding individuals that are reproductively isolated from other such populations. Therefore, understanding how reproductive barriers evolve between populations is essential for understanding the process of speciation. Hybrid incompatibility (e.g. hybrid sterility and lethality) is a common and strong reproductive barrier in nature, but few studies have molecularly identified its genetic basis. Here we report a lethal incompatibility between two wild-isolates of the nematode Caenorhabditis nouraguensis. Hybrid inviability results from the incompatibility between a maternally inherited cytoplasmic factor from each strain and a recessive nuclear locus from the other. We have excluded the possibility that maternally inherited endosymbiotic bacteria cause the incompatibility by treating both strains with tetracycline and show that hybrid death is unaffected. Furthermore, cytoplasmic-nuclear incompatibility commonly occurs between other wild-isolates, indicating that this is a significant reproductive barrier within C. nouraguensis. We hypothesize that the maternally inherited cytoplasmic factor is the mitochondrial genome and that mitochondrial dysfunction underlies hybrid death. This system has the potential to shed light on the dynamics of divergent mitochondrial-nuclear coevolution and its role in promoting speciation.

evolutionary biology↗

bioRxiv2017

Gene regulatory network rewiring by an adaptively evolving microRNA cluster in Drosophila

New miRNAs are evolutionarily important but their impact on existing biological networks remains unclear. We report the evolution of a microRNA cluster, mir-972C, that arose de novo and the subsequently rewired gene regulatory networks in Drosophila. Molecular evolution analyses revealed that mir-972C originated in the common ancestor of Drosophila where it comprises five old miRNAs. It subsequently recruited five new members in the melanogaster subgroup after conservative evolution for at least 50 million years. Population genetics analyses reveal that young and old mir-972C miRNAs evolved rapidly under positive selection in both seed and non-seed regions. Combining target prediction and cell transfection experiments, we find that sequence changes in individual mir-972C members resulted in extensive gene regulatory network divergence among D. melanogaster, D. simulans, and D. virilis, whereas the target pool of the cluster as a whole remains relatively conserved. Our results suggest that clustering of young and old miRNAs at the same locus broadens target repertoires, resulting in the gain of new targets without losing many old ones. This may facilitate the establishment of new miRNAs within existing regulatory networks.

evolutionary biology↗

bioRxiv2018

Evolution of preferences in group-structured populations: genes, guns, and culture

During human evolution, individuals interacted mostly within small groups that were connected by limited migration and sometimes by conflicts. Which preferences, if any, will prevail in such scenarios? Building on population biology models of spatially structured populations, and assuming individuals preferences to be their private information, we characterize those preferences that, once established, cannot be displaced by alternative preferences. We represent such uninvadable preferences in terms of fitness and in terms of material payoffs. At the fitness level, individuals can be regarded to act as if driven by a mix of self-interest and a Kantian motive that evaluates own behavior in the light of the consequences for own fitness if others adopted this behavior. This Kantian motive is borne out from (genetic or cultural) kin selection. At the material-payoff level, individuals act as if driven in part by self-interest and a Kantian motive (in terms of material payoffs), but also in part by other-regarding preferences towards other group members. This latter motive is borne out of group resource constraints and the risk of conflict with other groups. We show how group size, the migration rate, the risk of group conflicts, and cultural loyalty shape the relative strengths of these motives.\n\nJEL codesA12, A13, B52, C73, D01, D63, D64, D91.

evolutionary biology↗

bioRxiv2017

Base composition, speciation, and why the mitochondrial barcode precisely classifies

While its mechanism and biological significance are unknown, the utility of a short mitochondrial DNA sequence as a \"barcode\" providing accurate species identification has revolutionized the classification of organisms. Since highest accuracy was achieved with recently diverged species, hopes were raised that barcodes would throw light on the speciation process. Indeed, a failure of a maternally-donated, rapidly mutating, mitochondrial genome to coadapt its gene products with those of a paternally-donated nuclear genome could result in developmental failure, thus creating a post-zygotic barrier leading to reproductive isolation and sympatric branching into independent species. However, the barcode itself encodes a highly conserved, species-invariant, protein, and the discriminatory power resides in the non-amino acid specific bases of synonymous codons. It is here shown how the latter could register changes in the oligonucleotide frequencies of nuclear DNA that, when they fail to match in pairing meiotic chromosomes, could reproductively isolate the parents (whose hybrid is sterile) so launching a primary divergence into two species. It is proposed that, while not itself contributing to speciation, the barcode sequence provides an index of the nuclear DNA oligonucleotide frequencies that drive speciation.

evolutionary biology↗

bioRxiv2017

Evidence for "inter- and intraspecific horizontal genetic transfers" between anciently asexual bdelloid rotifers is explained by cross-contamination

Bdelloid rotifers are microscopic invertebrates thought to have evolved for millions of years without sexual reproduction. They have attracted the attention of biologists puzzled by the maintenance of sex among nearly all other eukaryotes. Bdelloid genomes have an unusually high proportion of horizontally acquired non-metazoan genes. This well-substantiated finding has invited speculation that homologous horizontal transfer between rotifers also may occur, perhaps even 'replacing' sex. A 2016 study in Current Biology claimed to supply evidence for this hypothesis. The authors sampled rotifers of the genus Adineta from natural populations and sequenced one mitochondrial and four nuclear loci. For several samples, species assignments were incongruent among loci, which the authors interpreted as evidence of \"interspecific genetic exchanges\". Here, we use sequencing chromatograms supplied by the authors to demonstrate that samples treated as individuals actually contained two or more divergent mitochondrial and ribosomal sequences, indicating contamination with DNA from additional animals belonging to the supposed \"donor species\". We also show that \"exchanged\" molecules share only 75% sequence homology, a degree of divergence incompatible with established mechanisms of recombination and genomic features of Adineta. These findings are parsimoniously explained by cross-contamination of tubes with animals or DNA from different species. Given the proportion of tubes contaminated in this way, we show by calculation that evidence for \"intraspecific horizontal exchange\" in the same dataset is explained by contamination with conspecific DNA. On the clear evidence of these analyses, the 2016 study provides no reliable support for the hypothesis of horizontal genetic transfer between or within these bdelloid species.

evolutionary biology↗

bioRxiv2017

Stability of subsystem solutions in agent-based models

The fact that relatively simple entities, such as particles or neurons, or even ants or bees or humans, give rise to fascinatingly complex behavior when interacting in large numbers is the hallmark of complex systems science. Agent-based models are frequently employed for modeling and obtaining a predictive understanding of complex systems. Since the sheer number of equations that describe the behavior of an entire agent-based model often makes it impossible to solve such models exactly, Monte Carlo simulation methods must be used for the analysis. However, unlike pairwise interactions among particles that typically govern solid-state physics systems, interactions among agents that describe systems in biology, sociology or the humanities often involve group interactions, and they also involve a larger number of possible states even for the most simplified description of reality. This begets the question: When can we be certain that an observed simulation outcome of an agent-based model is actually stable and valid in the large system-size limit? The latter is key for the correct determination of phase transitions between different stable solutions, and for the understanding of the underlying microscopic processes that led to these phase transitions. We show that a satisfactory answer can only be obtained by means of a complete stability analysis of subsystem solutions. A subsystem solution can be formed by any subset of all possible agent states. The winner between two subsystem solutions can be determined by the average moving direction of the invasion front that separates them, yet it is crucial that the competing subsystem solutions are characterized by a proper composition and spatiotemporal structure before the competition starts. We use the spatial public goods game with diverse tolerance as an example, but the approach has relevance for a wide variety of agent-based models.

evolutionary biology↗

bioRxiv2018

Population genetic tests for the direction and relative timing of introgression

Introgression is a pervasive biological process, and many statistical methods have been developed to infer its presence from genomic data. However, many of the consequences and genomic signatures of introgression remain unexplored from a methodological standpoint. Here, we develop a model for the timing and direction of introgression based on the multispecies network coalescent, and from it suggest new approaches for testing introgression hypotheses. We suggest two new statistics, D1 and D2, which can be used in conjunction with other information to test hypotheses relating to the timing and direction of introgression, respectively. D1 may find use in evaluating cases of homoploid hybrid speciation, while D2 provides a four-taxon test for polarizing introgression. Although analytical expectations for our statistics require a number of assumptions to be met, we show how simulations can be used to test hypotheses about introgression when these assumptions are violated. We apply the D1 statistic to genomic data from the wild yeast Saccharomyces paradoxus, a proposed example of homoploid hybrid speciation, demonstrating its use as a test of this model. These methods provide new and powerful ways to address questions relating to the timing and direction of introgression.

evolutionary biology↗

bioRxiv2017

The Rate Of Evolution Of Postmating-Prezygotic Reproductive Isolation In Drosophila

Reproductive isolation (RI) is an intrinsic aspect of species, as described in the Biological Species Concept. For that reason, the identification of the precise traits and mechanisms of RI, and the rates at which they evolve, is crucial to understanding how species originate and persist. Nonetheless, precise measurements of the magnitude of reproductive isolation are rare. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has carried out the study of the rates of evolution of postmating-prezygotic (PMPZ) barriers. We systematically measured the magnitude of two barriers to gene flow that act after mating occurs but before zygotic fertilization and also measured a premating (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of species within the Drosophila melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. We also describe seven new interspecific hybrids in the group. Our findings open up a large repertoire of tools that will enable researchers to manipulate hybrids and explore the genetic basis of interspecific differentiation, reproductive isolation, and speciation.

evolutionary biology↗