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bioRxiv2018

Ancestral Reconstruction of Protein Interaction Networks

The molecular and cellular basis of novelty is a major open question in evolutionary biology. Until very recently, the vast majority of cellular phenomena were so difficult to sample that cross-species studies of biochemistry were rare and comparative analysis at the level of biochemical systems was almost impossible. Recent advances in systems biology are changing what is possible, however, and comparative phylogenetic methods that can handle this new data are wanted. Here, we introduce the term \"phylogenetic latent variable models\" (PLVMs, pronounced \"plums\") for a class of models that has recently been used to infer the evolution of cellular states from systems-level molecular data, and develop a new parameterization and fitting strategy that is useful for comparative inference of biochemical networks. We deploy this new framework to infer the ancestral states and evolutionary dynamics of protein-interaction networks by analyzing >16,000 predominantly metazoan co-fractionation and affinity-purification mass spectrometry experiments. Based on these data, we estimate ancestral interactions across unikonts, broadly recovering protein complexes involved in translation, transcription, proteostasis, transport, and membrane trafficking. Using these results, we predict an ancient core of the Commander complex made up of CCDC22, CCDC93, C16orf62, and DSCR3, with more recent additions of COMMD-containing proteins in tetrapods. We also use simulations to develop model fitting strategies and discuss future model developments.

evolutionary biology↗
bioRxiv2016

Going down the rabbit hole: a review on how to link genome-wide data with ecology and evolution in natural populations

O_LICharacterizing species history and identifying loci underlying local adaptation is crucial in functional ecology, evolutionary biology, conservation and agronomy. The ongoing and constant improvement of next-generation sequencing (NGS) techniques has facilitated the production of an ever-increasing number of genetic markers across genomes of non-model species.\nC_LIO_LIThe study of variation in these markers across natural populations has deepened the understanding of how population history and selection act on genomes. Population genomics now provides tools to better integrate selection into a historical framework, and take into account selection when reconstructing demographic history. However, this improvement has come with a burst of analytical tools that can confuse users.\nC_LIO_LISuch confusion can limit the amount of information effectively retrieved from complex genomic datasets. In addition, the lack of a unified analytical pipeline impairs the diffusion of the most recent analytical tools into fields like conservation biology.\nC_LIO_LITo address this need, we describe possible analytical protocols and link these with more than 70 methods dealing with genome-scale datasets. We summarise the strategies they use to infer demographic history and selection, and discuss some of their limitations. A website listing these methods is available at www.methodspopgen.com.\nC_LI

Evolutionary Biology↗
bioRxiv2017

Stags, hawks, and doves: Social evolution theory and individual variation in cooperation

One of the triumphs of evolutionary biology is the discovery of robust mechanisms that promote the evolution of cooperative behaviors even when those behaviors reduce the fertility or survival of cooperators. Though these mechanisms, kin selection, reciprocity, and nonlinear payoffs to cooperation, have been extensively studied separately, investigating their joint effect on the evolution of cooperation has been more difficult. Moreover, how these mechanisms shape variation in cooperation is not well known. Such variation is crucial for understanding the evolution of behavioral syndromes and animal personality. Here, I use the tools of kin selection theory and evolutionary game theory to build a framework that integrates these mechanisms for pairwise social interactions. Using relatedness as a measure of the strength of kin selection, responsiveness as a measure of reciprocity, and synergy as a measure of payoff nonlinearity, I show how different combinations of these three parameters produce directional selection for or against cooperation or variation in levels of cooperation via balancing or diversifying selection. Moreover, each of these outcomes maps uniquely to one of four classic games from evolutionary game theory, which means that modulating relatedness, responsiveness, and synergy effectively transforms the payoff matrix from one the evolutionary game to another. Assuming that cooperation exacts a fertility cost on cooperators and provides a fertility benefit to social partners, a prisoners dilemma game and directional selection against cooperation occur when relatedness and responsiveness are low and synergy is not too positive. Enough positive synergy in these conditions generates a stag-hunt game and diversifying selection. High levels of relatedness or responsiveness turn cooperation from a fitness cost into a fitness benefit, which produces a mutualism game and directional selection for cooperation when synergy is not too negative. Sufficiently negative synergy in this case creates a hawk-dove game and balancing selection for cooperation. I extend the results with relatedness and synergy to larger social groups and show that how group size changes the effect of relatedness and synergy on selection for cooperation depends on how the per capita benefit of cooperation changes with group size. Together, these results provide a general framework with which to generate comparative predictions that can be tested using quantitative genetic techniques and experimental techniques that manipulate investment in cooperation. These predictions will help us understand both interspecific variation in cooperation as well as within-population and within-group variation in cooperation related to behavioral syndromes.

evolutionary biology↗
bioRxiv2016

Happens in the best of subfamilies: Replacement and internalisation of co-obligate Serratia endosymbionts in Lachninae aphids

Virtually all aphids maintain an obligate mutualistic symbiosis with bacteria from the Buchnera genus, which produce essential nutrients for their aphid hosts. Most aphids from the Lachninae subfamily have been consistently found to house additional endosymbionts, mainly Serratia symbiotica. This apparent dependence on secondary endosymbionts was proposed to have been triggered by the loss of the riboflavin biosynthetic capability by Buchnera in the Lachninae last common ancestor. However, an integral large-scale analysis of secondary endosymbionts in the Lachninae is still missing, hampering the interpretation of the evolutionary and genomic analyses of these endosymbionts. Here, we analysed the endosymbionts of selected representatives from seven different Lachninae genera and nineteen species, spanning four tribes, both by FISH (exploring the symbionts morphology and tissue tropism) and 16S rRNA gene sequencing. We demonstrate that all analysed aphids possess dual symbiotic systems, and while most harbour S. symbiotica, some have undergone symbiont replacement by other phylogenetically-distinct bacterial taxa. We found that these secondary associates display contrasting cell shapes and tissue tropism, and some appear to be lineage-specific. a scenario for symbiont establishment in the Lachninae, followed by changes in the symbionts tissue tropism and symbiont replacement events, thereby highlighting the extraordinary versatility of host-symbiont interactions.\n\nOriginality-Significance StatementA key question in evolutionary biology is that of how mutualism evolves. One way to approach this problem is to investigate recently-established mutualistic associations, particularly by comparing various symbiotic systems in closely related hosts. Here, we present a most comprehensive study to investigate co-obligate symbioses in aphids, focusing in the Lachninae subfamily. While most aphids keep an obligate vertically-transmitted association with intracellular Buchnera bacteria, some, such as members of the Lachninae subfamily, host an additional putative co-obligate symbiont. Thus, the Lachninae dual symbiotic systems offer a unique opportunity to understand the evolutionary dynamics of host-symbiont associations, in particularly how secondary symbionts become obligate and eventually may be replaced. Through genome sequencing of three aphid species belonging to distantly related tribes within the subfamily, we have previously corroborated that they have indeed established co-obligate mutualistic associations with the S. symbiotica secondary endosymbiotic bacterium. This was putatively facilitated by an ancient pseudogenisation of the riboflavin biosynthetic pathway in Buchnera, rendering it unable to provide the essential vitamin to the host. However, not all Lachninae members harbour S. symbiotica, some species being associated to at least four different bacterial taxa. To correctly interpret the genomic data and to understand the evolutionary dynamics of these symbiotic associations, a wide-range analysis of both the phylogenetic relations as well as of the secondary symbionts localisation within the bacteriome is needed. To tackle this, we have combined phylogenetic analyses of the symbionts 16S rRNA gene sequences and FISH microscopy, to understand the symbionts identity as well as the morphological characteristics and tissue tropism. The phylogenetic affinities and patterns of co-divergence of the symbionts, in combination with previously published genomic data, have enabled us to build an evolutionary scenario for the establishment, changes in tissue tropism such as \"stable\" internalisation into bacteriocytes, and replacements of the putative \"ancient\" secondary endosymbiont from the Lachninae last common ancestor. Also, we were able to determine through phylogenetic analyses that some putative co-obligate endosymbionts may have evolved from once facultative ones. The evolutionary framework presented here reveals a dynamic pattern for the more recent evolutionary history of these symbioses, including replacement and novel acquisition of phylogenetically different co-obligate symbionts. This study opens new research avenues on this symbiont-diverse subfamily, providing insight into how mutualism in endosymbiotic associations can evolve, and the role these bacteria have played in the species adaptation and even in the speciation process.

Evolutionary Biology↗
bioRxiv2017

Identifying drivers of parallel evolution: A regression model approach

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100045). Parallel evolution, defined as identical changes arising in independent populations, is often attributed to similar selective pressures favoring the fixation of identical genetic changes. However, some level of parallel evolution is also expected if mutation rates are heterogeneous across regions of the genome. Theory suggests that mutation and selection can have equal impacts on patterns of parallel evolution, however empirical studies have yet to jointly quantify the importance of these two processes. Here, we introduce several statistical models to examine the contributions of mutation and selection heterogeneity to shaping parallel evolutionary changes at the gene-level. Using this framework we analyze published data from forty experimentally evolved Saccharomyces cerevisiae populations. We can partition the effects of a number of genomic variables into those affecting patterns of parallel evolution via effects on the rate of arising mutations, and those affecting the retention versus loss of the arising mutations (i.e. selection). Our results suggest that gene-to-gene heterogeneity in both mutation and selection, associated with gene length, recombination rate, and number of protein domains drive parallel evolution at both synonymous and nonsynonymous sites. While there are still a number of parallel changes that are not well described, we show that allowing for heterogeneous rates of mutation and selection can provide improved predictions of the prevalence and degree of parallel evolution.\n\nData archival locationDryad, doi to be included later

evolutionary biology↗
bioRxiv2014

Bias and measurement error in comparative analyses: a case study with the Ornstein Uhlenbeck model

Phylogenetic comparative methods are increasingly used to give new insight into variation, causes and consequences of trait variation among species. The foundation of these methods is a suite of models that attempt to capture evolutionary patterns by extending the Brownian constant variance model. However, the parameters of these models have been hypothesised to be biased and only asymptotically behave in a statistically predictable way as datasets become large. This does not seem to be widely appreciated. We show that a commonly used model in evolutionary biology (the Ornstein-Uhlenbeck model) is biased over a wide range of conditions. Many studies fitting this model use datasets that are small and prone to substantial biases. Our results suggest that simulating fitted models and comparing with empirical results is critical when fitting OU and other extensions of the Brownian model.

Evolutionary Biology↗
bioRxiv2016

A Central Limit Theorem for Punctuated Equilibrium

Current evolutionary biology models usually assume that a phenotype undergoes gradual change. This is in stark contrast to biological intuition, which indicates that change can also be punctuated-the phenotype can jump. Such a jump can especially occur at speciation, i.e. dramatic change occurs that drives the species apart. Here we derive a Central Limit Theorem for punctuated equilibrium. We show that, if adaptation is fast, for weak convergence to hold, dramatic change has to be a rare event.\n\nAMS subject classification: 60F05, 60J70, 60J85, 62P10, 92B99

Evolutionary Biology↗
bioRxiv2016

The evolution of coercive policing in genetically mixed groups: the case of plasmid copy number control

Policing is a widespread mechanism regulating cooperation in both human and animal social groups. Policing can promote the evolution and maintenance of cooperation among non-relatives by tying the reproductive success of individuals to the efficiency and success of the group. In this paper, we investigate the evolution of reproductive policing using a multi-scale computational model inspired by the copy number control system of conjugative bacterial plasmids. Our results show that the repression of competition through policing can evolve across a very broad range of migration (plasmid conjugation) rates, improving system-level performance and bringing efficiency gains to the group beyond those achievable by pure self-restraint. Reproductive policing acts to increase genetic relatedness by reducing variation in group size which, in turn, reduces the heterogeneity of the plasmid population. When among-group migration is high, coercive policing strategies are favoured, characterized by high levels of policing coupled with relatively lower obedience. Coercive policing strategies preferentially limit the reproduction of rival lineages while, at the same time, maintaining effective collective reproductive control.\n\nAuthor SummaryThe emergence and maintenance of cooperation is a topic of great importance in evolutionary biology. The evolution of cooperation has been explained in the context of kin selection when there is sufficient genetic relatedness among interacting individuals. When there is insufficient relatedness, the presence of alternative mechanisms, such as mutual policing, can promote the evolution and maintenance of cooperation by tying the reproductive success of individual to the efficiency and success of the group. In this paper, we investigate the evolution of reproductive policing using an agent-based computational model inspired by a simple and elegant biological example: replication control among conjugative plasmids, a class of molecular symbionts of bacterial hosts. Our results show that the repression of competition through policing evolves and improves plasmid group performance beyond levels achievable by self-restraint, across a very broad range of migration rates. Under conditions of high migration (frequent conjugation), we observe the evolution of coercive policing strategies that limit the reproduction of rival lineages by investing disproportionately in policing relative to their obedience to the policing trait.

Evolutionary Biology↗
bioRxiv2018

Fitness-dependent recombination can be evolutionarily advantageous in diploids: a deterministic mutation-selection balance model

Recombinations omnipresence in nature is one of the most intriguing problems in evolutionary biology. The question of why recombination exhibits certain general features is no less interesting than that of why it exists at all. One such feature is recombinations fitness dependence (FD). The so far developed population-genetics models have focused on the evolution of FD recombination mainly in haploids, although the empirical evidence for this phenomenon comes mostly from diploids. Using numerical analysis of modifier models for infinite panmictic populations, we show here that FD recombination can be evolutionarily advantageous in diploids subjected to purifying selection. This advantage is associated with benefits from the differential rate of disruption of lower- vs higher-fitness genotypes, that can be manifested in systems with at least three selected loci. We also show that in systems with linked modifier, an additional contribution to the evolutionary advantage of FD recombination may come from fitness-dependence of the intensity of modifier linkage to the selected system, although the contribution of the last effect vanishes with tighter linkage within the selected system. We also show that in systems with three selected loci, FD recombination may give rise to negative crossover interference, which may be beneficial by itself. Yet, the role of such FD-induced crossover interference in the evolutionary advantage of FD recombination is minor. Remarkably, FD recombination was often favored in situations where any constant non-zero recombination was rejected, implying a relaxation of the rather strict constraints on major parameters (e.g., selection intensity and epistasis) required for the evolutionary advantage of non-zero recombination formulated by classical models.

evolutionary biology↗
bioRxiv2017

Preserving microsatellites? Conservation genetics of the giant Galapagos tortoise.

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100031).\n\nConservation policy in the giant Galapagos tortoise, an iconic endangered animal, has been assisted by genetic markers for [~]15 years: a dozen loci have been used to delineate thirteen (sub)species, between which hybridization is prevented. Here, comparative reanalysis of a previously published NGS data set reveals a conflict with traditional markers. Genetic diversity and population substructure in the giant Galapagos tortoise are found to be particularly low, questioning the genetic relevance of current conservation practices. Further examination of giant Galapagos tortoise population genomics is critically needed.

evolutionary biology↗
bioRxiv2015

A targeted subgenomic approach for phylogenomics based on microfluidic PCR and high throughput sequencing

Advances in high-throughput sequencing (HTS) have allowed researchers to obtain large amounts of biological sequence information at speeds and costs unimaginable only a decade ago. Phylogenetics, and the study of evolution in general, is quickly migrating towards using HTS to generate larger and more complex molecular datasets. In this paper, we present a method that utilizes microfluidic PCR and HTS to generate large amounts of sequence data suitable for phylogenetic analyses. The approach uses a Fluidigm microfluidic PCR array and two sets of PCR primers to simultaneously amplify 48 target regions across 48 samples, incorporating sample-specific barcodes and HTS adapters (2,304 unique amplicons per microfluidic array). The final product is a pooled set of amplicons ready to be sequenced, and thus, there is no need to construct separate, costly genomic libraries for each sample. Further, we present a bioinformatics pipeline to process the raw HTS reads to either generate consensus sequences (with or without ambiguities) for every locus in every sample or--more importantly--recover the separate alleles from heterozygous target regions in each sample. This is important because it adds allelic information that is well suited for coalescent-based phylogenetic analyses that are becoming very common in conservation and evolutionary biology. To test our subgenomic method and bioinformatics pipeline, we sequenced 576 samples across 96 target regions belonging to the South American clade of the genus Bartsia L. in the plant family Orobanchaceae. After sequencing cleanup and alignment, the experiment resulted in [~]25,300bp across 486 samples for a set of 48 primer pairs targeting the plastome, and [~]13,500bp for 363 samples for a set of primers targeting regions in the nuclear genome. Finally, we constructed a combined concatenated matrix from all 96 primer combinations, resulting in a combined aligned length of [~]40,500bp for 349 samples.

Evolutionary Biology↗
bioRxiv2015

Directional variation in evolution: consequences for the fitness landscape metaphor

The concept of a fitness landscape, which describes the relation between genotype (or phenotype) and fitness as a surface on which the population climbs uphill towards local peaks, is a central conceptual tool in evolutionary biology. Inherent in this metaphor is the assumption that the distance between any two points can be defined in the same way as for Euclidean space. However, many of the processes which generate genetic variation, such as gene duplication and lateral gene transfer, are not symmetric by nature, but occur more readily in one direction than the other. This asymmetry is also found in phenotypes, for reasons associated with the genotype-phenotype map and developmental constraints. This article provides an overview of of these processes and suggest how existing methods can be used for incorporating these asymmetric processes when visualising fitness landscapes.

Evolutionary Biology↗
bioRxiv2014

Quantifying the effects of anagenetic and cladogenetic evolution

An ongoing debate in evolutionary biology is whether phenotypic change occurs predominantly around the time of speciation or whether it instead accumulates gradually over time. In this work I propose a general framework incorporating both types of change, quantify the effects of speciational change via the correlation between species and attribute the proportion of change to each type. I discuss results of parameter estimation of Hominoid body size in this light. I derive mathematical formulae related to this problem, the probability generating functions of the number of speciation events along a randomly drawn lineage and from the most recent common ancestor of two randomly chosen tip species for a conditioned Yule tree. Additionally I obtain in closed form the variance of the distance from the root to the most recent common ancestor of two randomly chosen tip species.

Evolutionary Biology↗
bioRxiv2017

Dramatic evolution of body length due to post-embryonic changes in cell size in a newly discovered close relative of C. elegans

Understanding morphological diversity--and morphological constrainto--has been a central question in evolutionary biology since its inception. Nematodes of the genus Caenorhabditis, which contains the well-studied model system C. elegans, display remarkable morphological consistency in the face of extensive genetic divergence. Here, we provide a description of the broad developmental patterns of a recently discovered species, C. sp. 34, which was isolated from fresh figs in Okinawa and which is among the closest known relatives of C. elegans. C. sp. 34 displays an extremely large body size and can grow to be nearly twice as long as C. elegans and all other known members of the genus. Observations of the timing of developmental milestones reveal that C. sp. 34 develops about twice as slowly as C. elegans. Measurements of embryo and larval size show that the size difference between C. sp. 34 and C. elegans is largely due to post-embryonic events, particularly during the transition from larval to adult stages. This difference in size is not attributable to differences in germ line chromosome number or the number of somatic cells. The overall difference in body size is therefore largely attributable to changes in cell size via increased cytoplasmic volume. Because of its close relationship to C. elegans, the distinctness of C. sp. 34 provides an ideal system for the detailed analysis of evolutionary diversification. The context of over forty years of C. elegans developmental genetics also reveals clues into how natural selection and developmental constraint act jointly to promote patterns of morphological stasis and divergence in this group.

evolutionary biology↗
bioRxiv2018

Does Adaptive Protein Evolution Proceed by Large or Small Steps at the Amino Acid Level?

A longstanding question in evolutionary biology is the relative contribution of large and small effect mutations to the adaptive process. We have investigated this question in proteins by estimating the rate of adaptive evolution between all pairs of amino acids separated by one mutational step using a McDonald-Kreitman type approach and genome-wide data from several Drosophila species. We find that the rate of adaptive evolution is higher amongst amino acids that are more similar. This is partly due to the fact that the proportion of mutations that are adaptive is higher amongst more similar amino acids. We also find that the rate of neutral evolution between amino acids is higher amongst similar amino acids. Overall our results suggest that both the adaptive and non-adaptive evolution of proteins is dominated by substitutions between amino acids that are more similar.

evolutionary biology↗
bioRxiv2017

Inferring Genetic Interactions From Comparative Fitness Data

AO_SCPLOWBSTRACTC_SCPLOWDarwinian fitness is a central concept in evolutionary biology. In practice, however, it is hardly possible to measure fitness for all genotypes in a natural population. Here, we present quantitative tools to make inferences about epistatic gene interactions when the fitness landscape is only incompletely determined due to imprecise measurements or missing observations. We demonstrate that genetic interactions can often be inferred from fitness rank orders, where all genotypes are ordered according to fitness, and even from partial fitness orders. We provide a complete characterization of rank orders that imply higher order epistasis. Our theory applies to all common types of gene interactions and facilitates comprehensive investigations of diverse genetic interactions. We analyzed various genetic systems comprising HIV-1, the malaria-causing parasite Plasmodium vivax, the fungus Aspergillus niger, and the TEM-family of {beta}-lactamase associated with antibiotic resistance. For all systems, our approach revealed higher order interactions among mutations.

evolutionary biology↗
bioRxiv2017

Maintenance of Polymorphism in Spatially Heterogeneous Environments: An Experimental Test of Hard and Soft Selection

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100020). Predicting and managing contemporary adaption requires a proper understanding of the determinants of genetic variation. Spatial heterogeneity of the environment may stably maintain polymorphism when habitat contribution to the next generation can be considered independent of the degree of adaptation of local populations within habitats (i.e., under soft selection). In contrast, when habitats contribute proportionally to the mean fitness of the populations they host (hard selection), polymorphism is not expected to be maintained by selection. Although mathematically established decades ago, this prediction had never been properly explored. Here we provide an experimental test in which polymorphic populations of Escherichia coli growing in heterogeneous habitats were exposed to hard and soft selection regimes. As predicted by theory, polymorphism was longer preserved under soft selection. Complementary tests established that soft selection slowed down fixation processes and could even protect polymorphism on the long term by providing a systematic advantage to rare genotypes.

evolutionary biology↗
bioRxiv2018

Increasing phylogenetic stochasticity at high elevations on summits across a remote North American wilderness

PREMISE OF THE STUDYAt the intersection of ecology and evolutionary biology, community phylogenetics can provide insights into overarching biodiversity patterns, particularly in remote and understudied ecosystems. To understand community assembly of the high-alpine flora of the Sawtooth National Forest, USA, we analyzed phylogenetic structure within and between nine summit communities.\n\nMETHODSWe used high-throughput sequencing to supplement existing data and infer a nearly completely sampled community phylogeny of the alpine vascular flora. We calculated mean nearest taxon distance (MNTD) and mean pairwise distance (MPD) to quantify phylogenetic divergence within summits, and assed how maximum elevation explains phylogenetic structure. To evaluate similarities between summits we quantified phylogenetic turnover, taking into consideration micro-habitats (talus vs. meadows).\n\nKEY RESULTSWe found different patterns of community phylogenetic structure within the six most species-rich orders, but across all vascular plants phylogenetic structure was largely no different from random. There was a significant negative correlation between elevation and tree-wide phylogenetic diversity (MPD) within summits: significant overdispersion degraded as elevation increased. Between summits we found high phylogenetic turnover, which was driven by greater niche heterogeneity on summits with alpine meadows.\n\nCONCLUSIONSThis study provides further evidence that stochastic processes shape the assembly of vascular plant communities in the high-alpine at regional scales. However, order-specific patterns suggest adaptations may be important for assembly of specific sectors of the plant tree of life. Further studies quantifying functional diversity will be important to disentangle the interplay of eco-evolutionary processes that likely shape broad community phylogenetic patterns in extreme environments.

evolutionary biology↗