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bioRxiv2017

The Prevalence And Benefits Of Admixture During Species Invasions: A Role For Epistasis?

Species introductions often bring together genetically divergent source populations, resulting in genetic admixture. This geographic reshuffling of diversity has the potential to generate favorable new genetic combinations, facilitating the establishment and invasive spread of introduced populations. Observational support for the superior performance of admixed introductions has been mixed, however, and the broad importance of admixture to invasion questioned. Under most underlying mechanisms, admixtures benefits should be expected to increasewith greater divergence among and lower genetic diversity within source populations. We use a literature survey to quantify the prevalence of admixture and evaluate whether it occurrs under circumstances predicted to be mostbeneficial to introduced species. We find that 39% of species are reported to be admixed when introduced. Admixed introductions come from sources with a wide range of genetic variation, but are disproportionately absent where there is high genetic divergence among native populations. We discuss multiple potential explanations for these patterns, but note that negative epistatic interactions should be expected at high divergence amongpopulations (outbreeding depression). As a case study, we experimentally cross source populations differing in divergence in the invasive plant Centaurea solstitialis. We find many positive (heterotic) interactions, but fitness benefits decline and are ultimately negative at high source divergence, with patterns suggestingcyto-nuclear epistasis. We conclude that admixture is common in species introductions and often happens under conditions expected to be beneficial to invaders, but that these conditions may be constrained by predictable negativegenetic interactions, potentially explaining conflicting evidence for admixture's benefits to invasion.

evolutionary biology↗

bioRxiv2017

Disentangling The Effects Of Selection And Loss Bias On Gene Dynamics

We combine mathematical modelling of genome evolution with comparative analysis of prokaryotic genomes to estimate the relative contributions of selection and intrinsic loss bias to the evolution of different functional classes of genes and mobile genetic elements (MGE). An exact solution for the dynamics of gene family size was obtained under a linear duplication-transfer-loss model with selection. With the exception of genes involved in information processing, particularly translation, which are maintained by strong selection, the average selection coefficient for most non-parasitic genes is low albeit positive, compatible with the observed positive correlation between genome size and effective population size. Free-living microbes evolve under stronger selection for gene retention than parasites. Different classes of MGE show a broad range of fitness effects, from the nearly neutral transposons to prophages, which are actively eliminated by selection. Genes involved in anti-parasite defense, on average, incur a fitness cost to the host that is at least as high as the cost of plasmids. This cost is probably due to the adverse effects of autoimmunity and curtailment of horizontal gene transfer caused by the defense systems and selfish behavior of some of these systems, such as toxin-antitoxin and restriction-modification modules. Transposons follow a biphasic dynamics, with bursts of gene proliferation followed by decay in the copy number that is quantitatively captured by the model. The horizontal gene transfer to loss ratio, but not the duplication to loss ratio, correlates with genome size, potentially explaining the increased abundance of neutral and costly elements in larger genomes.\n\nSIGNIFICANCEEvolution of microbes is dominated by horizontal gene transfer and the incessant host-parasite arms race that promotes the evolution of diverse anti-parasite defense systems. The evolutionary factors governing these processes are complex and difficult to disentangle but the rapidly growing genome databases provide ample material for testing evolutionary models. Rigorous mathematical modeling of evolutionary processes, combined with computer simulation and comparative genomics, allowed us to elucidate the evolutionary regimes of different classes of microbial genes. Only genes involved in key informational and metabolic pathways are subject to strong selection whereas most of the others are effectively neutral or even burdensome. Mobile genetic elements and defense systems are costly, supporting the understanding that their evolution is governed by the same factors.

evolutionary biology↗

bioRxiv2017

Dissecting HIV Virulence: Heritability Of Setpoint Viral Load, CD4+ T Cell Decline And Per-Parasite Pathogenicity

Pathogen strains may differ in virulence because they attain different loads in their hosts, or because they induce different disease-causing mechanisms independent of their load. In evolutionary ecology, the latter is referred to as \"per-parasite pathogenicity\". Using viral load and CD4+ T cell measures from 2014 HIV-1 subtype B infected individuals enrolled in the Swiss HIV Cohort Study, we investigated if virulence -- measured as the rate of decline of CD4+ T cells -- and per-parasite pathogenicity are heritable from donor to recipient. We estimated heritability by donor-recipient regressions applied to 196 previously identified transmission pairs, and by phylogenetic mixed models applied to a phylogenetic tree inferred from HIV pol sequences. Regressing the CD4+ T cell declines and per-parasite pathogenicities of the transmission pairs did not yield heritability estimates significantly different from zero. With the phylogenetic mixed model, however, our best estimate for the heritability of the CD4+ T cell decline is 17% (5%-30%), and that of the per-parasite pathogenicity is 17% (4%-29%). Further, we confirm that the set-point viral load is heritable, and estimate a heritability of 29% (12%-46%). Interestingly, the pattern of evolution of all these traits differs significantly from neutrality, and is most consistent with stabilizing selection for the set-point viral load, and with directional selection for the CD4+ T cell decline and the per-parasite pathogenicity. Our analysis shows that the viral genetype affects virulence mainly by modulating the per-parasite pathogenicity, while the indirect effect via the set-point viral load is minor.

evolutionary biology↗

bioRxiv2017

STRIDE: Species Tree Root Inference From Gene Duplication Events

The correct interpretation of a phylogenetic tree is dependent on it being correctly rooted. A gene duplication event at the base of a clade of species is synapamorphic, and thus excludes the root of the species tree from that clade. We present STRIDE, a fast, effective, and outgroup-free method for species tree root inference from gene duplication events. STRIDE identifies sets of well-supported gene duplication events from cohorts of gene trees, and analyses these events to infer a probability distribution over an unrooted species tree for the location of the true root. We show that STRIDE infers the correct root of the species tree for a large range of simulated and real species sets. We demonstrate that the novel probability model implemented in STRIDE can accurately represent the ambiguity in species tree root assignment for datasets where information is limited. Furthermore, application of STRIDE to inference of the origin of the eukaryotic tree resulted in a root probability distribution that was consistent with, but unable to distinguish between, leading hypotheses for the origin of the eukaryotes. In summary, STRIDE is a fast, scalable, and effective method for species tree root inference from genome scale data.

evolutionary biology↗

bioRxiv2017

CRISPR/Cas9 Mutation Of A Gonad-Expressed Opsin Prevents Jellyfish Light-Induced Spawning

Across the animal kingdom, environmental light cues are widely involved in regulating gamete release, but the molecular and cellular bases of the photoresponsive mechanisms are poorly understood. In hydrozoan jellyfish, spawning is triggered by dark-light or light-dark transitions acting on the gonad, and is mediated by oocyte maturation-inducing neuropeptide hormones (MIHs) released from the ectoderm. We determined in Clytia hemisphaerica that blue-cyan light triggers spawning in isolated gonads. A candidate opsin (Opsin9) was found co-expressed with MIH within specialised ectodermal cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, a phenotype reversible by synthetic MIH. Gamete maturation and release in Clytia is thus regulated by gonadal photosensory-neurosecretory cells that secrete MIH in response to light via Opsin9. Similar cells in ancestral eumetazoans may have allowed tissue-level photo-regulation of diverse behaviours, a feature elaborated in cnidarians in parallel with expansion of the opsin gene family.

evolutionary biology↗

bioRxiv2017

Tragedy Of The Commons In The Chemostat

We present a proof of principle for the phenomenon of the tragedy of the commons that is at the center of many theories on the evolution of cooperation. We establish the tragedy in the context of a general chemostat model with two species, the cooperator and the cheater. Both species have the same growth rate function and yield constant, but the cooperator allocates a portion of the nutrient uptake towards the production of a public good -the \"Commons\" in the Tragedy-which is needed to digest the externally supplied nutrient. The cheater on the other hand does not produce this enzyme, and allocates all nutrient uptake towards its own growth. We prove that when the cheater is present initially, both the cooperator and the cheater will eventually go extinct, hereby confirming the occurrence of the tragedy. We also show that without the cheater, the cooperator can survive indefinitely, provided that at least a low level of public good or processed nutrient is available initially. Our results provide a predictive framework for the analysis of cooperator-cheater dynamics in a powerful model system of experimental evolution.

evolutionary biology↗

bioRxiv2017

Diet And Life Stage Associated Remodeling Of Lipid Metabolism Regulation In The Duplicated Atlantic Salmon Genome

Atlantic salmon migrates from rivers to sea to feed, grow and develop gonads before returning to spawn in freshwater. These habitat shifts require great phenotypic plasticity. To address the unresolved question of how the shift in diet between fresh and saltwater affects the regulation of metabolic function, we fed salmon contrasting diets in each of the two life stages. Combining transcriptomics with comparative genomics, we found that lipid metabolism undergoes a concerted shift between fresh- and saltwater stages. Lipogenesis and lipid transport become less active in liver after transition to saltwater, while genes for lipid uptake in gut are more expressed in lipid-rich seawater environments. We assess how the whole-genome duplication that gave rise to the salmonids has impacted the evolution of lipid metabolism, and find signatures of pathway-specific selection pressure on gene duplicates, as well as a limited number of cases of increased gene dosage.

evolutionary biology↗

bioRxiv2017

Re-Evaluating Evolution In The HIV Reservoir

Despite antiretroviral therapy (ART), a latent reservoir of replication-competent HIV-1 persists in resting memory CD4+ T-cells and precludes cure1-6. Lorenzo-Redondo et al.7 analyzed HIV-1 sequences collected from three individuals during the first six months of ART, discovered specific patterns of sequence evolution, and concluded that viral replication persists during therapy. We believe these evolutionary patterns are artifacts of rapidly decaying viral subpopulations present during the first months of therapy and are not characteristic of the long-lived reservoir. The study therefore provides no evidence that ongoing replication is an additional barrier to cure for treated individuals who consistently maintain low viral loads.

evolutionary biology↗

bioRxiv2017

Thirty-five experimental fisheries reveal the mechanisms of selection

Fisheries have been described as large-scale evolutionary experiments; yet such \"experiments\" tend to be poorly replicated and therefore lack the predictive power essential for designing appropriate management strategies to minimize the effects of fisheries-induced selection. Large-scale removal of non-native trout from 35 montane lakes in California provided repeated experimental fisheries that allowed us to explore how environmental parameters affect the three potential contributors to overall selection: the fitness-trait correlation, trait variability, and fitness variability. Our results demonstrate that fishing rapidly altered the size structure of harvested populations, and that the magnitude of change was primarily driven by the fitness-trait correlation (net selectivity). Fishing-induced selection was repeatable overall but was also influenced by environmental (lake size and quality) and demographic (size structure) parameters. Decomposing fishing-induced selection into its key components can improve the management of stocks experiencing fishing-induced selection by identifying the drivers of selection and therefore the appropriate target for management.

evolutionary biology↗

bioRxiv2017

General Environmental Heterogeneity As The Explanation Of Sexuality? Comparative Study Shows That Ancient Asexual Taxa Are Associated With Both Biotically And Abiotically Homogeneous Environments

Ecological theories of sexual reproduction assume that sexuality is advantageous in certain conditions, for example, in biotically or abiotically more heterogeneous environments. Such theories thus could be tested by comparative studies. However, the published results of these studies are rather unconvincing. Here we present the results of a new comparative study based solely on the ancient asexual clades. The association with biotically or abiotically homogeneous environments in these asexual clades was compared with the same association in their sister, or closely related, sexual clades. Using the conservative definition of ancient asexuals (i.e. age > 1 million years), we found six pairs for which relevant ecological data are available. The difference between the homogeneity type of environment associated with the sexual and asexual species was then compared in an exact binomial test. Based on available literature, the results showed that the vast majority of ancient asexual clades tend to be associated with biotically or abiotically, biotically, and abiotically more homogeneous environments than their sexual controls. In the exploratory part of the study, we found that the ancient asexuals often have durable resting stages, enabling life in subjectively homogeneous environments, live in the absence of intense biotic interactions, and are very often sedentary, inhabiting benthos and soil. The consequences of these findings for the ecological theories of sexual reproduction are discussed.

evolutionary biology↗

bioRxiv2017

Protein Evolution Depends On Multiple Distinct Population Size Parameters

That population size affects the fate of new mutations arising in genomes, modulating both how frequently they arise and how efficiently natural selection is able to filter them, is well established. It is therefore clear that these distinct roles for population size that characterize different processes should affect the evolution of proteins and need to be carefully defined. Empirical evidence is consistent with a role for demography in influencing protein evolution, supporting the idea that functional constraints alone do not determine the composition of coding sequences.\n\nGiven that the relationship between population size, mutant fitness and fixation probability has been well characterized, estimating fitness from observed substitutions is well within reach with well-formulated models. Molecular evolution research has, therefore, increasingly begun to leverage concepts from population genetics to quantify the selective effects associated with different classes of mutation. However, in order for this type of analysis to provide meaningful information about the intra- and inter-specific evolution of coding sequences, a clear definition of concepts of population size, what they influence, and how they are best parameterized is essential.\n\nHere, we present an overview of the many distinct concepts that \"population size\" and \"effective population size\" may refer to, what they represent for studying proteins, and how this knowledge can be harnessed to produce better specified models of protein evolution.

evolutionary biology↗

bioRxiv2017

Drift-Induced Selection Between Male And Female Heterogamety

Evolutionary transitions between male and female heterogamety are common in both vertebrates and invertebrates. Theoretical studies of these transitions have found that, when all genotypes are equally fit, continuous paths of intermediate equilibria link the two sex chromosome systems. This observation has led to a belief that neutral evolution along these paths can drive transitions, and that arbitrarily small fitness differences among sex chromosome genotypes can determine the system to which evolution leads. Here, we study stochastic evolutionary dynamics along these equilibrium paths. We find non-neutrality, both in transitions retaining the ancestral pair of sex chromosomes and in those creating a new pair. In fact, substitution rates are strongly biased in favor of dominant sex determining chromosomes, which fix with higher probabilities than mutations of no effect. Using diffusion approximations, we show that this non-neutrality is a result of drift-induced selection operating at every point along the equilibrium paths: stochastic jumps off the paths return, on average, with a directional bias in favor of the dominant segregating sex chromosome. Our results offer novel explanations for the ubiquity of transitions between male and female heterogamety and the preponderance of dominant major sex determining genes.

evolutionary biology↗

bioRxiv2017

Evaluating Fast Maximum Likelihood-Based Phylogenetic Programs Using Empirical Phylogenomic Data Sets

Phylogenetics has witnessed dramatic increases in the sizes of data matrices assembled to resolve branches of the tree of life, motivating the development of programs for fast, yet accurate, inference. For example, several different fast programs have been developed in the very popular maximum likelihood framework, including RAxML/ExaML, PhyML, IQ-TREE, and FastTree. Although these four programs are widely used, a systematic evaluation and comparison of their performance using empirical genome-scale data matrices has so far been lacking. To address this question, we evaluated these four programs on 19 empirical phylogenomic data sets from diverse animal, plant, and fungal lineages with respect to likelihood maximization, tree topology, and computational speed. For single-gene tree inference, we found that the more exhaustive and slower strategies (ten searches per alignment) outperformed faster strategies (one tree search per alignment) using RAxML, PhyML, or IQ-TREE. Interestingly, single-gene trees inferred by the three programs yielded comparable coalescent-based species tree estimations. For concatenation-based species tree inference, IQ-TREE consistently achieved the best-observed likelihoods for all data sets, and RAxML/ExaML was a close second. In contrast, PhyML often failed to complete concatenation-based analyses, whereas FastTree was the fastest but generated lower likelihood values and more dissimilar tree topologies in both types of analyses. Finally, data matrix properties, such as the number of taxa and the strength of phylogenetic signal, sometimes substantially influenced the relative performance of the programs. Our results provide real-world gene and species tree phylogenetic inference benchmarks to inform the design and execution of large-scale phylogenomic data analyses.

evolutionary biology↗

bioRxiv2017

Evolution of bird communication signals: transference between signals mediated by sensory drive

Animals communicate using signals perceived via multiple sensory modalities but usually invest more heavily in one of type of signal. This pattern, observed by Darwin1 and many researchers since, led to development of the transfer hypothesis (see also transferal effect2 and tradeoff hypothesis3,4), which predicts a negative relationship between investment in different signaling modalities dictated by the relative costs and benefits of each. One factor that influences costs and benefits, and is central to the sensory drive hypothesis5 posed to account for signal evolution, is the suitability of the environment for different types of signals. Movement into a dark habitat, for example, should favor investment in acoustic over visual signals. We use phylogenetic comparative methods to analyze the joint effect of transfer and sensory drive on plumage and song variation in 52 species of a large radiation of passerine birds, the New World warblers (Parulidae), and to estimate temporal patterns in the accumulation of differences in visual and vocal signals and habitat along the evolutionary history of this lineage. We found evidence for the predicted negative correlations between a variety of song and plumage traits that vary with habitat type. Plumage contrast to background and chromatic diversity were both negatively related to syllable variety when vegetation structure was a covariate: birds with a greater variety of song syllables and less colorful plumages live in closed or darker habitats. Also as predicted, achromatic or brightness diversity was related to vegetation structure. In addition, disparity-through-time analyses showed that when one set of traits (i.e. songs or colors) diversified at a relatively high rate the other did not, as predicted by the transfer hypothesis. Our results show that sensory drive influences the transfer of investment between traits in different sensory modalities. This interaction between mechanisms shaping signals may be a major determinant in the evolution of animal communication.

evolutionary biology↗

bioRxiv2017

Mechanical And Tactile Incompatibilities Cause Reproductive Isolation Between Two Young Damselfly Species

External male reproductive structures have received considerable attention as an early-acting cause of reproductive isolation (RI), because the morphology of these structures often evolves rapidly between populations. This presents the potential for mechanical incompatibilities with heterospecific female structures during mating and could thus prevent interbreeding between nascent species. Although such mechanical incompatibilities have received little empirical support as a common cause of RI, the potential for mismatch of reproductive structures to cause RI due to incompatible species-specific tactile cues has not been tested. We tested the importance of mechanical and tactile incompatibilities in RI between Enallagma anna and E. carunculatum, two damselfly species that diverged within the past ~250,000 years and currently hybridize in a sympatric region. We quantified 19 prezygotic and postzygotic RI barriers using both naturally occurring and lab-reared damselflies. We found incomplete mechanical isolation between the two pure species and between hybrid males and pure species females. Interestingly, where mechanical isolation was incomplete, females showed greater resistance and refusal to mate with hybrid or heterospecific males compared to conspecific males, which suggests that tactile incompatibilities involving male reproductive structures can influence female mating decisions and form a strong barrier to gene flow in early stages of speciation.

evolutionary biology↗

bioRxiv2017

Reviving A Lost Species: The Case Of The Floreana Galapagos Giant Tortoise Chelonoidis elephantopus

Species are being lost at an unprecedented rate due to human-driven environmental changes. The cases in which species declared extinct can be revived are rare. However, here we report that a remote volcano in the Galapagos Islands hosts many giant tortoises with high ancestry from a species previously declared as extinct: Chelonoidis elephantopus or the Floreana tortoise. Of 150 individuals with distinctive morphology sampled from the volcano, genetic analyses revealed that 65 had C. elephantopus ancestry and thirty-two were translocated from the volcanos slopes to a captive breeding center. A genetically informed captive breeding program now being initiated will, over the next decades, return C. elephantopus tortoises to Floreana Island to serve as engineers of the islands ecosystems. Ironically, it was the haphazard translocations by mariners killing tortoises for food centuries ago that created the unique opportunity to revive this \"lost\" species today.

evolutionary biology↗

bioRxiv2017

Characterization Of Imprinted Genes In Rice Reveals Post-Fertilization Regulation And Conservation At Some Loci Of Imprinting In Plant Species

Genomic imprinting is an epigenetic phenomenon by which certain genes display monoallelic expression in a parent-of-origin-dependent manner. Hundreds of imprinted genes have been identified from several plant species. Here we identified, with a high level of confidence, 208 imprinted candidates from rice. Imprinted genes of rice showed limited association to the transposable elements, which is contrast to the findings in Arabidopsis. Generally, imprinting of rice is conserved within species, but intraspecific variations were confirmed here. Imprinting between cultivated rice and wild rice are likely similar. The imprinted genes of rice do not show significant selective signatures overall, which suggests that domestication imposes limited evolutionary effects on genomic imprinting of rice. Though the conservation of imprinting in plants is limited, here we prove that some loci tend to be imprinted in different species. In addition, our results suggest that differential epigenetic regulation between parental alleles can be established either prior to or post-fertilization. The imprinted 24-nt small RNAs, but not the 21-nt ones, likely involve the regulation of imprinting in an opposite parental-allele targeting manner. Together, our findings suggest that regulation of imprinting can be very diverse, and genomic imprinting as well as imprinted genes have essential evolutionary and biological significance.

plant biology↗

bioRxiv2017

Parasite-Driven Replacement Of A Sexual By A Closely Related Asexual Taxon In Nature

Asexual species are thought to suffer more from coevolving parasites than related sexuals. Yet, this prediction may be modulated by the fact that closely related sexuals and asexuals often differ in respects other than reproductive mode. Here, we follow the frequency dynamics of sexual and asexual Daphnia pulex in a natural pond that was initially dominated by sexuals. However, coinciding with an epidemic of a microsporidian parasite infecting both sexuals and asexuals, the pond was rapidly taken over by the initially rare asexuals. We experimentally confirm that asexuals are less susceptible and also suffer less from the parasite once infected. These results show the ecological replacement of a sexual taxon by a closely related asexual taxon, as driven by parasites. We suggest that this replacement is, however, not directly connected with the reproductive mode, but rather due to the recent introduction and invasive nature of the asexuals studied.

evolutionary biology↗