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bioRxiv2017

POUMM: An R-package for Bayesian Inference of Phylogenetic Heritability

AO_SCPLOWBSTRACTC_SCPLOWPhylogenetic comparative methods have been used to model trait evolution, to test selection versus neutral hypotheses, to estimate optimal trait-values, and to quantify the rate of adaptation towards these optima. Several authors have proposed algorithms calculating the likelihood for trait evolution models, such as the Ornstein-Uhlenbeck (OU) process, in time proportional to the number of tips in the tree. Combined with gradient-based optimization, these algorithms enable maximum likelihood (ML) inference within seconds, even for trees exceeding 10,000 tips. Despite its useful statistical properties, ML has been criticised for being a point estimator prone to getting stuck in local optima. As an elegant alternative, Bayesian inference explores the entire information in the data and compares it to prior knowledge but, usually, runs in much longer time, even for small trees. Here, we propose an approach to use the full potential of ML and Bayesian inference, while keeping the runtime within minutes. Our approach combines (i) a new algorithm for parallel likelihood calculation; (ii) a previously published method for adaptive Metropolis sampling. In principle, the strategy of (i) and (ii) can be applied to any likelihood calculation on a tree which proceeds in a pruning-like fashion leading to enormous speed improvements. As a showcase, we implement the phylogenetic Ornstein-Uhlenbeck mixed model (POUMM) in the form of an easy-to-use and highly configurable R-package. In addition to the above-mentioned usage of comparative methods, the POUMM allows to estimate non-heritable variance and phylogenetic heritability. Using simulations and empirical data from 487 mammal species, we show that the POUMM is far more reliable in terms of unbiased estimates and false positive rate for stabilizing selection, compared to its alternative - the non-mixed Ornstein-Uhlenbeck model, which assumes a fully heritable and perfectly measurable trait. Further, our analysis reveals that the phylogenetic mixed model (PMM), which assumes neutral evolution (Brownian motion) can be a very unstable estimator of phylogenetic heritability, even if the Brownian motion assumption is only weakly violated. Our results prove the need for a simultaneous account for selection and non-heritable variance in phylogenetic evolutionary models and challenge stabilizing selection hypotheses stated in numerous macro-evolutionary studies.

evolutionary biology↗

bioRxiv2017

Predicting metabolic adaptation from networks of mutational paths

Competition for substrates is a ubiquitous selection pressure faced by microbes, yet intracellular trade-offs can prevent cells from metabolizing every type of available substrate. Adaptive evolution is constrained by these trade-offs, but their consequences for the repeatability and predictability of evolution are unclear. Here we develop an eco-evolutionary model with a metabolic trade-off to generate networks of mutational paths in microbial communities and show that these networks have descriptive and predictive information about the evolving communities. We find that long-term outcomes, including community collapse, diversity, and cycling, have characteristic evolutionary dynamics that determine the entropy, or repeatability, of mutational paths. Although reliable prediction of evolutionary outcomes from environmental conditions is difficult, graph-theoretic properties of the mutational networks enable accurate prediction even from incomplete observations. In conclusion, we present a novel methodology for analyzing adaptive evolution and report that the dynamics of adaptation are a key variable for predictive success.

evolutionary biology↗

bioRxiv2017

Master manipulation continued: feminizing Wolbachia endosymbiont distorts sex chromosome inheritance

Genomes are vulnerable to selfish genetic elements that enhance their own transmission often at the expense of host fitness. Examples are cytoplasmic elements such as maternally inherited bacteria that cause feminization, male-killing, parthenogenesis and cytoplasmic incompatibility. We demonstrate, for the first time, that segregation distortion, a phenomenon so far seen only for nuclear genetic elements, can also be caused by a cytoplasmic element, the ubiquitous endosymbiotic bacterium Wolbachia. For Eurema mandarina butterfly lineages with a Z0 sex chromosome constitution, we provide direct and conclusive evidence that Wolbachia induces production of all-female progeny by a dual role: the compensation for the female-determining function that is absent in Z0 lineages (feminization) and the prevention of maternal sex chromosome inheritance to offspring as a specific type of segregation distortion. Therefore, our findings highlight that both sex determination and chromosome inheritance -- crucially important developmental processes of higher eukaryotes -- can be manipulated by cytoplasmic parasites.

evolutionary biology↗

bioRxiv2017

Segregation lift: A general mechanism for the maintenance of polygenic variation under seasonally fluctuating selection.

Most natural populations are affected by seasonal changes in temperature, rainfall, or resource availability. Seasonally fluctuating selection could potentially make a large contribution to maintaining genetic polymorphism in populations. However, previous theory suggests that the conditions for multi-locus polymorphism are restrictive. Here we explore a more general class of models with multi-locus seasonally fluctuating selection in diploids. In these models, loci first contribute additively to a seasonal score, with a dominance parameter determining the relative contributions of heterozygous and homozygous loci. The seasonal score is then mapped to fitness via a monotonically increasing function, thereby accounting for epistasis. Using mathematical analysis and individual-based simulations, we show that stable polymorphism at many loci is possible if currently favored alleles are sufficiently dominant with respect to the additive seasonal score (but not necessarily with respect to fitness itself). This general mechanism, which we call \"segregation lift\", operates for various genotype-to-fitness maps and includes the previously known mechanism of multiplicative selection with marginal overdominance as a special case. We show that segregation lift may arise naturally in situations with antagonistic pleiotropy and seasonal changes in the relative importance of traits for fitness. Segregation lift is not affected by problems of genetic load and is robust to differences in parameters across loci and seasons. Under segregation lift, loci can exhibit conspicuous seasonal allele-frequency fluctuations, but often fluctuations may also be small and hard to detect. Via segregation lift, seasonally fluctuating selection might contribute substantially to maintaining genetic variation in natural populations.

evolutionary biology↗

bioRxiv2017

The mutational decay of male and hermaphrodite competitive fitness in the androdioecious nematode C. elegans, in which males are naturally rare

Androdioecious Caenorhabditis have a high frequency of self-compatible hermaphrodites and a low frequency of males. The effects of mutations on male fitness are of interest for two reasons. First, when males are rare, selection on male-specific mutations is less efficient than in hermaphrodites. Second, males may present a larger mutational target than hermaphrodites because of the different ways in which fitness accrues in the two sexes.\n\nWe report the first estimates of male-specific mutational effects in an androdioecious organism. The rate of male-specific inviable or sterile mutations is [≤] 5 x 10-4/generation, below the rate at which males would be lost solely due to those kinds of mutations. The rate of mutational decay of male competitive fitness is ~0.17%/generation; that of hermaphrodite competitive fitness is ~0.11%/generation. The point estimate of ~1.5X faster rate of mutational decay of male fitness is nearly identical to the same ratio in Drosophila. Estimates of mutational variance (VM) for male mating success and competitive fitness are not significantly different from zero, whereas VM for hermaphrodite competitive fitness is similar to that of non-competitive fitness. The discrepancy between the two sexes is probably due to the greater inherent variability of mating relative to internal self-fertilization.

evolutionary biology↗

bioRxiv2017

Widespread paleopolyploidy, gene tree conflict, and recalcitrant relationships among the carnivorous Caryophyllales

O_LIThe carnivorous members of the large, hyperdiverse Caryophyllales (e.g. Venus flytrap, sundews and Nepenthes pitcher plants) represent perhaps the oldest and most diverse lineage of carnivorous plants. However, despite numerous studies seeking to elucidate their evolutionary relationships, the early-diverging relationships remain unresolved.\nC_LIO_LITo explore the utility of phylogenomic data sets for resolving relationships among the carnivorous Caryophyllales, we sequenced ten transcriptomes, including all the carnivorous genera except those in the rare West African liana family (Dioncophyllaceae). We used a variety of methods to infer the species tree, examine gene tree conflict and infer paleopolyploidy events.\nC_LIO_LIPhylogenomic analyses support the monophyly of the carnivorous Caryophyllales, with an origin of 68-83 mya. In contrast to previous analyses recover the remaining non-core Caryophyllales as non-monophyletic, although there are multiple reasons this result may be spurious and node supporting this relationship contains a significant amount gene tree discordance. We present evidence that the clade contains at least seven independent paleopolyploidy events, previously debated nodes from the literature have high levels of gene tree conflict, and taxon sampling influences topology even in a phylogenomic data set.\nC_LIO_LIOur data demonstrate the importance of carefully considering gene tree conflict and taxon sampling in phylogenomic analyses. Moreover, they provide a remarkable example of the propensity for paleopolyploidy in angiosperms, with at least seven such events in a clade of less than 2500 species.\nC_LI

evolutionary biology↗

bioRxiv2017

A mechanistic model for the evolution of multicellularity

Through a mechanistic approach we investigate the formation of aggregates of variable sizes, accounting mechanisms of aggregation, dissociation, death and reproduction. In our model, cells can produce two metabolites, but the simultaneous production of both metabolites is costly in terms of fitness. Thus, the formation of larger groups can favor the aggregates to evolve to a configuration where division of labor arises. It is assumed that the states of the cells in a group are those that maximizes organismal fitness. In the model it is considered that the groups can grow linearly, forming a chain, or compactly keeping a roughly spherical shape. Starting from a population consisting of single-celled organisms, we observe the formation of groups with variable sizes and usually much larger than two-cell aggregates. Natural selection can favor the formation of large groups, which allows the system to achieve new and larger fitness maxima.

evolutionary biology↗

bioRxiv2017

Asymmetric evolution of the transcription profiles and cis-regulatory sites contributes to the retention of transcription factor duplicates

Transcription factors (TFs) play a key role in regulating plant development and response to environmental stimuli. While most genes revert to single copy after a duplication event, transcription factors are retained at a significantly higher rate. However, it is unclear why TF duplicates have higher rates of retention relative to other genes. In this study, we compared three types of features (expression, sequence, and conservation) of retained TFs following whole genome duplication (WGD) events to genes with other functions, using Arabidopsis thaliana as a model. We found that gene function groups with higher maximum expression but lower mean expression tended to have higher duplicate retention rate post WGD, though TFs in particular are retained more often than would be expected based on the features examined. Conversely, expression of individual genes was not associated with duplication, but sequence conservation was. Furthermore, we found that the evolution of TF expression patterns and cis-regulatory cites favors the partitioning of ancestral states among the resulting duplicates. In particular, we found that one duplicate retains the majority of ancestral expression and cis-regulatory sites, while the \"non-ancestral\" duplicate was enriched for novel regulatory sites. To investigate how this pattern of partitioning pattern evolved, we modeled the retention of ancestral states in duplicate pairs using a system of differential equations. Our findings indicate that duplicate pairs evolve to a partitioned state more often than away from it, which in combination with accumulation of new regulatory sites in non-ancestral duplicates, suggest that selection favors partitioning via neofunctionalization.\n\nAuthor SummaryGene expression is controlled by regulatory proteins known as transcription factors. These factors control how an organism develops and responds to its environment. The evolution of transcription factor functions also contributes to the emergence of new species and crop domestication. In plants, new transcription factors mainly arise due to polyploidy, multiplication of the genome. Although most duplicated copies are lost following a genome duplication event, transcription factors are exceptional because they are often kept. Furthermore, we found that transcription factor duplicates that tend to diverge in how they are expressed and regulated in an unusual way where one copy mirrors the original, pre-duplication functional states of the ancestral gene, while the other loses the ancestral status and instead accumulates novel regulatory sites. Our results suggest these duplicate transcription factors may have been kept because one copy preserve ancestral function while the other has evolved new ones.

evolutionary biology↗

bioRxiv2017

Evolution of age-specific decline in stress phenotypes is driven by both antagonistic pleiotropy and mutation accumulation

Efforts to more fully understand and test evolutionary theories of aging have produced distinct predictions for mutation accumulation (MA) and antagonistic pleiotropy (AP) mechanisms. We build on these predictions through the use of association mapping and investigation of the change in additive effects of polymorphisms across age and among traits for multiple stress response phenotypes. We found that cold stress survival with acclimation, cold stress survival without acclimation, and starvation resistance declined with age and that changes in the genetic architecture of each phenotype were consistent with MA predictions. We used a novel test for MA and AP by calculating the additive effect of polymorphisms across ages and found support for both MA and AP mechanisms in the age-related decline in stress tolerance. These patterns suggest both MA and AP contribute to age-related change in stress response and highlight the utility of association mapping to identify genetic shifts across age.

evolutionary biology↗

bioRxiv2017

Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness

The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insects bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit-genes concordant with its reduction of diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, since these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.

evolutionary biology↗

bioRxiv2017

Functional Characterization of the Morpheus Gene Family

DATA ACCESSThe cDNA sequences reported in this paper have been deposited in the GenBank database (accession numbers): KF175165-KF175225 and BACs accession numbers that are used in this study: AC148621, AC190226, AC097327, AC097332, AC190226, AC097333, AC145401, AC187943, AC166855, AC166597, AC167295, AC235773, AC202644, and AC234805.\n\nABSTRACTThe burst of segmental duplications during human and great ape evolution focuses on a set of \"core\" duplicons encoding great-ape-specific gene families. Characterization of these gene families is complicated by their high copy number, incomplete sequence, and polymorphic nature. We investigate the structure, transcriptional diversity, and protein localization of the nuclear pore complex-interacting protein (NPIP) or Morpheus gene family. The corresponding core, LCRA, encodes one of the most rapidly evolving genes in the human genome; LCRA has expanded to ~20 copies from a single ancestral locus in Old World monkey and is associated with most of the recurrent chromosome 16 microdeletions implicated in autism and mental retardation. Phylogenetic analysis and cDNA sequencing suggest two distinct subfamilies or subtypes, NPIPA and NPIPB. The latter expanded recently within the great apes due to a series of structural changes within the canonical gene structure. Among Old World monkey, we observe a testis-specific pattern of expression that contrasts with the ubiquitous pattern observed among human tissues. This change in the expression profile coincides with the structural events that reshaped the structure and organization of the gene family. Most of the expressed human copies are capable of producing an open reading frame. Immunofluorescence analyses of the morpheus genes showed a primary localization to both the nucleus and its periphery. We show that morpheus genes may be upregulated upon pI:C treatment and find evidence of human autoantibodies produced against the NPIPB protein, raising the possibility that morpheus genes may be related to immune- or autoimmune-related function.

evolutionary biology↗

bioRxiv2017

Habitat Fragmentation Causes Coevolutionary Burning Spots

Habitat fragmentation increasingly threatens the services provided by natural communities and ecosystem worldwide. An understanding of the underlying eco-evolutionary processes in natural settings is lacking, yet critical to realistic and sustainable conservation. Through integrating the multivariate genetic, biotic and abiotic facets of a natural community network experiencing various degrees of habitat fragmentation, we provide unique insights into the processes underlying community functioning in real, natural conditions. The focal community network comprises a parasitic butterfly of conservation concern, and its two obligatory host species, a plant and an ant. We show that fragmentation of butterfly habitat has the potential to impair the balance between dispersal and coevolution. This process can cause coevolutionary burning spots of decreased genetic diversity and therefore of increased extinction risk. We stress that ignoring such eco-evolutionary feed-backs inherent to the very functioning of natural communities can strongly impact their persistence.\n\nOne Sentence SummaryCommunities under threat of habitat fragmentation suffer increased extinction risk through coevolutionary overheating.

evolutionary biology↗

bioRxiv2017

Why concatenation fails in the anomaly zone

AbstrctGenome-scale sequencing has been of great benefit in recovering species trees, but has not provided final answers. Despite the rapid accumulation of molecular sequences, resolving short and deep branches of the tree of life has remained a challenge, and has prompted the development of new strategies that can make the best use of available data. One such strategy - the concatenation of gene alignments - can be successful when coupled with many tree estimation methods, but has also been shown to fail when there are high levels of incomplete lineage sorting. Here, we focus on the failure of likelihood-based methods in retrieving a rooted, asymmetric four-taxon species tree from concatenated data when the species tree is in or near the anomaly zone - a region of parameter space where the most common gene tree does not match the species tree because of incomplete lineage sorting. First, we use coalescent theory to prove that most informative sites will support the species tree in the anomaly zone, and that as a consequence maximum-parsimony succeeds in recovering the species tree from concatenated data. We further show that maximum-likelihood tree estimation from concatenated data fails both inside and outside the anomaly zone, and that this failure is unconnected to the frequency of the most common gene tree. We provide support for a hypothesis that likelihood-based methods fail in and near the anomaly zone because discordant sites on the species tree have a lower likelihood than those that are discordant on alternative topologies. Our results confirm and extend previous reports of the failure and success of likelihood- and parsimony-based methods, and highlight avenues for future work improving the performance of methods aimed at recovering species tree.

evolutionary biology↗

bioRxiv2017

Random Drift With A Determined Outcome: A Parsimonious Null Model OfNeanderthal Replacement By Modern Humans Via Neutral Species Drift

The processes that led to the demise of the Neanderthals and their replacement by modern humans have been the object of speculation, research, and heated debate. Most hypotheses fall into one of two categories: one highlights the role of climate change, epidemics, or other environmental pressures in the Neanderthals demise, and the other attributes it to direct or indirect competition with modern humans, who seem to have occupied the same ecological niche. The latter are based on the assumption that modern humans benefited from some selective advantage over Neanderthals that led to the latters extinction. We show that a scenario that includes migration and selectively neutral species drift can explain the Neanderthals replacement and is in line with the archaeological evidence. Our model offers a parsimonious alternative to those that invoke external factors or selective advantage, and can represent a null hypothesis in assessing such alternatives. We show that for a wide range of parameters this hypothesis cannot be rejected. Moreover, we suggest that although selection and environmental factors may or may not have played a role in the interspecies dynamics of the Neanderthals and modern humans, the eventual outcome of these dynamics, the replacement of the Neanderthals, was the result of the hominid migration dynamics at the end of the middle Paleolithic, namely repeated migration of modern humans from Africa into the Levant and Europe.\n\nSignificance statementMultiple factors have been proposed as possible drivers of the extinction of the Neanderthals and their replacement by modern humans circa 40,000 years ago: climate change, epidemics, and - most prominently - a selective advantage, such as superior cognitive capacity of modern humans over Neanderthals. We propose an alternative model that includes only migration of modern humans out of Africa into the Levant and Europe. We show that, given that the two species occupied a similar ecological niche, modern humans were destined to replace the Neanderthals even under a neutral scenario in which neither species has a selective advantage.

evolutionary biology↗

bioRxiv2017

Evolution of Animal Neural Systems

Nervous systems are one of the most spectacular products of evolution. Their provenance and evolution have been an area of interest and often intense debate since the late 19th century. The genomics era has provided researchers with a new set of tools with which to study the early evolution of neurons, and recent progress on the molecular evolution of the first neurons has been both exciting and frustrating. It has become increasingly obvious that genomic data is often insufficient to reconstruct complex phenotypes in deep evolutionary time. We review this recent progress and its attendant challenges, and suggest ways forward.

evolutionary biology↗

bioRxiv2017

Postmating sexual selection and the enigmatic jawed genitalia of Callosobruchus subinnotatus

Insect genitalia exhibit rapid divergent evolution. Truly extraordinary structures have evolved in some groups, presumably as a result of post-mating sexual selection. To increase our understanding of this phenomenon, we studied the function of one such structure. The male genitalia of Callosobruchus subinnotatus (Coleoptera: Bruchinae) contain a pair of jaw-like structures with unknown function. Here, we used phenotypic engineering to ablate the teeth on these jaws. We then experimentally assessed the effects of ablation of the genital jaws on mating duration, ejaculate weight, male fertilization success and female fecundity, using a double-mating experimental design. We predicted that copulatory wounding in females should be positively related to male fertilization success. However, we found no significant correlation between genital tract scarring in females and male fertilization success. Male fertilization success was, however, positively related to the amount of ejaculate transferred by males and negatively related to female ejaculate dumping. Ablation of male genital jaws did not affect male relative fertilization success but resulted in a reduction in female egg production. Our results suggest that postmating sexual selection in males indeed favors these genital jaws, but not primarily through an elevated relative success in sperm competition but by increasing female egg production.

evolutionary biology↗

bioRxiv2017

Flexible Parental Care: Uniparental Incubation In Biparentally Incubating Shorebirds

Recent findings suggest that relative investment of females and males into parental care depends on the populations adult sex-ratio. For example, all else being equal, males should be the more caring sex if the sex ratio is male biased. Whether such outcomes are evolutionary fixed (i.e. related to the species typical sex-ratio) or whether they arise through flexible responses of individuals to the current population sex-ratio remains unclear. Nevertheless, a flexible response might be limited by evolutionary history when one sex loses the ability to care or when a single parent cannot successfully care. Here, we demonstrate that after the disappearance of one parent, individuals from 8 out of 15 biparentally incubating shorebird species were able to incubate uniparentally for 1-19 days (median = 3, N = 69). Such uniparental phases often resembled the incubation rhythm of species with obligatory uniparental incubation. Although it has been suggested that females of some shorebirds desert their brood after hatching, our findings indicate that either sex may desert prior to hatching. Strikingly, in 27% of uniparentally incubated clutches - from 5 species - we document successful hatching. Our data thus reveal the potential for a flexible switch from biparental to uniparental care.

evolutionary biology↗

bioRxiv2017

Dual RNA-seq Reveals No Plastic Transcriptional Response Of The Coccidian Parasite Eimeria falciformis To Host Immune Defences

BackgroundParasites can either respond to differences in immune defenses that exist between individual hosts plastically or, alternatively, follow a genetically canalized (\"hard wired\") program of infection. Assuming that large-scale functional plasticity would be discernible in the parasite transcriptome we have performed a dual RNA-seq study of the full lifecycle of Eimeria falciformis using infected mice with different immune status (e.g. naive versus immune animals) as models for coccidian infections.\n\nResultsWe compared parasite and host transcriptomes (dual transcriptome) between naive and challenge infected mice, as well as between immune competent and immune deficient ones. Mice with different immune competence show transcriptional differences as well as differences in parasite reproduction (oocyst shedding). Broad gene categories represented by differently abundant host genes indicate enrichments for immune reaction and tissue repair functions. More specifically, TGF-beta, EGF, TNF and IL-1 and IL-6 are examples of functional annotations represented differently depending on host immune status. Much in contrast, parasite transcriptomes were neither different between Coccidia isolated from immune competent and immune deficient mice, nor between those harvested from naive and challenge infected mice. Instead, parasite transcriptomes have distinct profiles early and late in infection, characterized largely by biosynthesis or motility associated functional gene groups, respectively. Extracellular sporozoite and oocyst stages showed distinct transcriptional profiles and sporozoite transcriptomes were found enriched for species specific genes and likely pathogenicity factors.\n\nConclusionWe propose that the niche and host-specific parasite E. falciformis uses a genetically canalized program of infection. This program is likely fixed in an evolutionary process rather than employing phenotypic plasticity to interact with its host. In turn this might (negatively) influence the ability of the parasite to use different host species and (positively or negatively) influence its evolutionary potential for adaptation to different hosts or niches.

evolutionary biology↗