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bioRxiv2016

Formation of novel PRDM9 allele by indel events as possible trigger for tarsier-anthropoid split

PRDM9 is currently the sole speciation gene found in vertebrates causing hybrid sterility probably due to incompatible alleles. Its role in defining the double strand break loci during the meiotic prophase I is crucial for proper chromosome segregation. Therefore, the rapid turnover of the loci determining zinc finger array seems to be causative for incompatibilities. We here investigated the zinc finger domain-containing exon of PRDM9 in 23 tarsiers. Tarsiers, the most basal extant haplorhine primates, exhibit two frameshifting indels at the 5-end of the array. The first mutation event interrupts the reading frame and function while the second compensates both. The fixation of this peculiar allele variant in tarsiers led to hypothesize that de- and reactivation of the zinc finger domain drove the speciation in early haplorhine primates. Moreover, the high allelic diversity within Tarsius point to multiple effects of genetic drift reflecting their phylogeographic history since the Miocene.

Evolutionary Biology↗

bioRxiv2016

Complex heterochrony underlies the evolution of hermaphrodite self-fertility and sex allocation in experimental C. elegans populations

Hermaphroditic organisms are common both in plants and animals, and have served as key models to study the evolution of sex allocation. Despite extensive past research, the specific developmental mechanisms by which hermaphrodite sex allocation can evolve remain largely unknown. To address this problem, we here use experimental evolution of Caenorhabditis elegans hermaphrodite-male populations to directly quantify changes in germline and somatic development that underlie adaptive shifts in hermaphrodite sex allocation associated with the evolution of improved self-fertility. Specifically, we test whether the evolution of hermaphrodite sex allocation is due to heterochrony, i.e. evolutionary changes in the relative timing of developmental processes.\n\nWe show that the experimental evolution of improved hermaphrodite self-fertility occurred through complex modification of a suite of developmental and reproductive traits: increased sperm production, accelerated oogenesis and ovulation rates, and increased embryo retention in utero. The experimental evolution of increased sperm production delayed entry into oogenesis - as expected, given the sequentially coupled production of spermatogenesis and oogenesis. Surprisingly, however, delayed oogenesis onset did not delay reproductive maturity, nor did it trade-off with gamete or embryo size. Comparing developmental dynamics of germline and soma indicates that the evolution of increased sperm production did not delay reproductive maturity due to a globally accelerated larval development during the period of spermatogenesis.\n\nWe conclude that the integration of multiple heterochronic events in gametogenesis and soma can explain the experimental evolution of hermaphrodite sex allocation and self-fertility. Our results thus support the idea that heterochrony can represent a specific mechanism that explains the maintenance of partial selfing in natural populations with mixed reproduction modes and different forms of hermaphroditism. More generally, our results provide a quantitative perspective on how natural selection can operate on developmental characters - and their integration - during the evolution of life history at the population level.

Evolutionary Biology↗

bioRxiv2016

Phylogenetic incongruence and the origins of cardenolide-resistant forms of Na+,K+-ATPase in North American Danaus butterflies

Rapid species radiations can obscure phylogenetic relationships between even distantly related species and lead to incorrect evolutionary inferences. For this reason, we examined evolutionary relationships among the three North American milkweed butterflies, Danaus plexippus, D. gilippus and D. eresimus using >400 orthologous gene sequences assembled from transcriptome data. Contrary to previous phylogenetic assessments, our results indicate that D. plexippus and D. eresimus are the sister taxa among these species. This result explains many previously noted phylogenetic incongruences such as an amino acid substitution in the sodium-potassium pump (Na+,K+-ATPase) of D. eresimus and D. plexippus, which increases resistance to the toxins found in these butterflies host plants. In accordance with a rapid radiation of Danaus butterflies, we also find evidence that both incomplete lineage sorting and post-speciation genetic exchange have contributed significantly to the evolutionary histories of these species. Furthermore, our findings suggest that D. plexippus is highly derived both morphologically and behaviorally.

Evolutionary Biology↗

bioRxiv2016

Microevolution of Bank Voles (Myodes glareolus) at Neutral and Immune Related Genes During Multiannual Dynamic Cycles: Consequences for Puumala hantavirus Epidemiology

Understanding how host dynamics, including variations of population size and dispersal, may affect the epidemiology of infectious diseases through ecological and evolutionary processes is an active research area. Here we focus on a bank vole (Myodes glareolus) metapopulation surveyed in Finland between 2005 and 2009. Bank vole is the reservoir of Puumala hantavirus (PUUV), the agent of nephropathia epidemica (NE, a mild form of hemorrhagic fever with renal symptom) in humans. M glareolus populations experience multiannual density fluctuations that may influence the level of genetic diversity maintained in bank voles, PUUV prevalence and NE occurrence. We examine bank vole metapopulation genetics at presumably neutral markers and immune-related genes involved in susceptibility to PUUV (Tnf-promoter, Mhc-Drb, Tlr4, Tlr7 and Mx2 gene) to investigate the links between population dynamics, microevolutionary processes and PUUV epidemiology. We show that genetic drift slightly and transiently affects neutral and adaptive genetic variability within the metapopulation. Gene flow seems to counterbalance its effects during the multiannual density fluctuations. The low abundance phase may therefore be too short to impact genetic variation in the host, and consequently viral genetic diversity. Environmental heterogeneity does not seem to affect vole gene flow, which might explain the absence of spatial structure previously detected in PUUV in this area. Besides, our results suggest the role of vole dispersal on PUUV circulation through sex-specific and density-dependent movements. We find little evidence of selection acting on immune-related genes within this metapopulation. Footprint of positive selection is detected at Tlr-4 gene in 2008 only. We observe marginally significant associations between Mhc-Drb haplotypes and PUUV serology, and between Mx2 genotype and PUUV genogroups. These results show that microevolutionary changes and PUUV epidemiology in this metapopulation are mainly driven by neutral processes, although the relative effects of neutral and adaptive forces could vary temporally with density fluctuations.

Evolutionary Biology↗

bioRxiv2016

Do aye-ayes echolocate? Studying convergent genomic evolution in a primate auditory specialist

Several taxonomically distinct mammalian groups - certain microbats and cetaceans (e.g. dolphins) - share both morphological adaptations related to echolocation behavior and strong signatures of convergent evolution at the amino acid level across seven genes related to auditory processing. Aye-ayes (Daubentonia madagascariensis) are nocturnal lemurs with a derived auditory processing system. Aye-ayes tap rapidly along the surfaces of dead trees, listening to reverberations to identify the mines of wood-boring insect larvae; this behavior has been hypothesized to functionally mimic echolocation. Here we investigated whether there are signals of genomic convergence between aye-ayes and known mammalian echolocators. We developed a computational pipeline (BEAT: Basic Exon Assembly Tool) that produces consensus sequences for regions of interest from shotgun genomic sequencing data for non-model organisms without requiring de novo genome assembly. We reconstructed complete coding region sequences for the seven convergent echolocating bat-dolphin genes for aye-ayes and another lemur. Sequences were compared in a phylogenetic framework to those of bat and dolphin echolocators and appropriate non-echolocating outgroups. Our analysis reaffirms the existence of amino acid convergence at these loci among echolocating bats and dolphins; we also detected unexpected signals of convergence between echolocating bats and both mice and elephants. However, we observed no significant signal of amino acid convergence between aye-ayes and echolocating bats and dolphins; our results thus suggest that aye-aye tap-foraging auditory adaptations represent distinct evolutionary innovations. These results are also consistent with a developing consensus that convergent behavioral ecology is not necessarily a reliable guide to convergent molecular evolution.

Evolutionary Biology↗

bioRxiv2016

The effects of population size histories on estimates of selection coefficients from time-series genetic data

AO_SCPCAPBSTRACTC_SCPCAPMany approaches have been developed for inferring selection coefficients from time series data while accounting for genetic drift. However, the improvement in inference accuracy that can be attained by modeling drift is unknown. Here, by comparing maximum likelihood estimates of selection coefficients that account for the true population size history with estimates that ignore drift, we address the following questions: how much can modeling the population size history improve estimates of selection coefficients? How much can mis-inferred population sizes hurt inferences of selection coefficients? We conduct our analysis under the discrete Wright-Fisher model by deriving the exact probability of an allele frequency trajectory in a population of time-varying size and we replicate our results under the diffusion model by extending the exact probability of a frequency trajectory derived by Steinrucken et al. (2014) to the case of a piecewise constant population. For both the discrete Wright-Fisher and diffusion models, we find that ignoring drift leads to estimates of selection coefficients that are nearly as accurate as estimates that account for the true population history, even when population sizes are small and drift is high. In populations of time-varying size, estimates of selection coefficients that ignore drift are similar in accuracy to estimates that rely on crude, yet reasonable, estimates of the population history. These results are of interest because inference methods that ignore drift are widely used in evolutionary studies and can be many orders of magnitude faster than methods that account for population sizes.

Evolutionary Biology↗

bioRxiv2016

Retrotransposon proliferation coincident with the evolution of dioecy in Asparagus

Current phylogenetic sampling reveals that dioecy and an XY sex chromosome pair evolved once or possibly twice in the genus Asparagus. Although there appear to be some lineage-specific polyploidization events, the base chromosome number of 2n=2x=20 is relatively conserved across the Asparagus genus. Regardless, dioecious species tend to have larger genomes than hermaphroditic species. Here we test whether this genome size expansion in dioecious species is related to a polyploidization and subsequent chromosome fusion or retrotransposon proliferation in dioecious species. We first estimate genome sizes or use published values for four hermaphrodites and four dioecious species distributed across the phylogeny and show that dioecious species typically have larger genomes than hermaphroditic species. Utilizing a phylogenomic approach we find no evidence for ancient polyploidization contributing to increased genome sizes of sampled dioecious species. We do find support for an ancient whole genome duplication event predating the diversification of the Asparagus genus. Repetitive DNA content of the four hermaphroditic and four dioecious species was characterized based on randomly sampled whole genome shotgun sequencing and common elements were annotated. Across our broad phylogenetic sampling, Ty-1 Copia retroelements in particular have undergone a marked proliferation in dioecious species. In the absence of a detectable whole genome duplication event, retrotransposon proliferation is the most likely explanation for the precipitous increase in genome size in dioecious Asparagus species.

Evolutionary Biology↗

bioRxiv2016

On the (un-)predictability of a large intragenic fitness landscape

The study of fitness landscapes, which aims at mapping genotypes to fitness, is receiving ever-increasing attention. Novel experimental approaches combined with NGS methods enable accurate and extensive studies of the fitness effects of mutations - allowing us to test theoretical predictions and improve our understanding of the shape of the true underlying fitness landscape, and its implications for the predictability and repeatability of evolution.\n\nHere, we present a uniquely large multi-allelic fitness landscape comprised of 640 engineered mutants that represent all possible combinations of 13 amino-acid changing mutations at six sites in the heat-shock protein Hsp90 in Saccharomyces cerevisiae under elevated salinity. Despite a prevalent pattern of negative epistasis in the landscape, we find that the global fitness peak is reached via four positively epistatic mutations. Combining traditional and extending recently proposed theoretical and statistical approaches, we quantify features of the global multi-allelic fitness landscape. Using subsets of the data, we demonstrate that extrapolation beyond a known part of the landscape is difficult owing to both local ruggedness and amino-acid specific epistatic hotspots, and that inference is additionally confounded by the non-random choice of mutations for experimental fitness landscapes.\n\nAuthor SummaryThe study of fitness landscapes is fundamentally concerned with understanding the relative roles of stochastic and deterministic processes in adaptive evolution. Here, the authors present a uniquely large and complete multi-allelic intragenic fitness landscape of 640 systematically engineered mutations in yeast Hsp90. Using a combination of traditional and recently proposed theoretical approaches, they study the accessibility of the global fitness peak, and the potential for predictability of the fitness landscape topography. They report local ruggedness of the landscape and the existence of epistatic hotspot mutations, which together make extrapolation and hence predictability inherently difficult, if mutation-specific information is not considered.

Evolutionary Biology↗

bioRxiv2016

Selective pressures on C4 photosynthesis evolution in grasses through the lens of optimality

CO2, temperature, water availability and light intensity were all potential selective pressures to propel the initial evolution and global expansion of C4 photosynthesis over the last 30 million years. To tease apart how the primary selective pressures varied along this evolutionary trajectory, we coupled photosynthesis and hydraulics models while optimizing photosynthesis over stomatal resistance and leaf/fine-root allocation. We further examined the importance of resource (e.g. nitrogen) reallocation from the dark to the light reactions during and after the initial formation of C4 syndrome. We show here that the primary selective pressures--all acting upon photorespiration in C3 progenitors--changed through the course of C4 evolution. The higher stomatal resistance and leaf-to-root allocation ratio enabled by the C4 carbon-concentrating mechanism led to a C4 advantage without any change in hydraulic properties, but selection on nitrogen reallocation varied. Water limitation was the primary driver for the initial evolution of C4 25-32 million years ago, and could positively select for C4 evolution with atmospheric CO2 as high as 600 ppm. Under these high CO2 conditions, nitrogen reallocation was necessary. Low CO2 and light intensity, but not nitrogen reallocation, were the primary drivers during the global radiation of C4 5-10 MYA. Finally, our results suggest that identifying the predominate selective pressures at the time C4 first evolved within a lineage should help explain current biogeographical distributions.\n\nStatement of authorshipHZ, BH and EA conceptualized the study. HZ and EA built the model, HZ and BH put the idea in a general evolutionary context, HZ performed the modeling work and analyzed output data. HZ wrote the first draft, BH and EA contributed substantially to revisions.\n\nSignificance StatementC4 photosynthesis pathway had evolved more than 60 times independently across the terrestrial plants through mid-Oligocene (~30 MYA) and diversified at late Miocene (5 to 10 MYA). We use an optimal physiology model to examine the primary selective pressures along the evolutionary history. Water limitation was the primary driver for C4 evolution from the initial evolutionary events 25-32 MYA until CO2 became low enough to, along with light intensity, drive the global radiation of C4 5-10 MYA. This modeling framework can be used to investigate evolution of other physiological traits (e.g. N reallocation, hydraulics) after the initial formation of C4 syndrome, which contributed to further increasing productivity of C4 in historical and current environmental conditions.

Evolutionary Biology↗

bioRxiv2016

An experimental evaluation of drug-induced mutational meltdown as an antiviral treatment strategy

The rapid evolution of drug resistance remains a critical public health concern. The treatment of influenza A virus (IAV) has proven particularly challenging, due to the ability of the virus to develop resistance against current antivirals and vaccines. Here we evaluate a novel antiviral drug therapy, favipiravir, for which the mechanism of action in IAV involves an interaction with the viral RNA-dependent RNA polymerase resulting in an effective increase in the viral mutation rate. We utilized an experimental evolution framework, combined with novel population genetic method development for inference from time-sampled data, in order to evaluate the effectiveness of favipiravir against IAV. Evaluating whole genome polymorphism data across fifteen time points under multiple drug concentrations and in controls, we present the first evidence for the ability of viral populations to effectively adapt to low concentrations of favipiravir. In contrast, under high concentrations, we observe population extinction, indicative of mutational meltdown. We discuss the observed dynamics with respect to the evolutionary forces at play and emphasize the utility of evolutionary theory to inform drug development.

Evolutionary Biology↗

bioRxiv2016

On the importance of skewed offspring distributions and background selection in viral population genetics

Many features of virus populations make them excellent candidates for population genetic study, including a very high rate of mutation, high levels of nucleotide diversity, exceptionally large census population sizes, and frequent positive selection. However, these attributes also mean that special care must be taken in population genetic inference. For example, highly skewed offspring distributions, frequent and severe population bottleneck events associated with infection and compartmentalization, and strong purifying selection all affect the distribution of genetic variation but are often not taken in to account. Here, we draw particular attention to multiple-merger coalescent events and background selection, discuss potential mis-inference associated with these processes, and highlight potential avenues for better incorporating them in to future population genetic analyses.

Evolutionary Biology↗

bioRxiv2016

Did viruses evolve as a distinct supergroup from common ancestors of cells?

The evolutionary origins of viruses according to marker gene phylogenies, as well as their relationships to the ancestors of host cells remains unclear. In a recent article Nasir and Caetano-Anolles reported that their genome-scale phylogenetic analyses identify an ancient origin of the \"viral supergroup\" (Nasir et al (2015) A phylogenomic data-driven exploration of viral origins and evolution. Science Advances, 1(8):e1500527). It suggests that viruses and host cells evolved independently from a universal common ancestor. Examination of their data and phylogenetic methods indicates that systematic errors likely affected the results. Reanalysis of the data with additional tests shows that small-genome attraction artifacts distort their phylogenomic analyses. These new results indicate that their suggestion of a distinct ancestry of the viral supergroup is not well supported by the evidence.

Evolutionary Biology↗

bioRxiv2016

Allele Surfing Promotes Microbial Adaptation from Standing Variation

The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from soft selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource-limited populations to cope with environmental challenges.

Evolutionary Biology↗

bioRxiv2016

Estimating seven coefficients of pairwise relatedness using population genomic data

Population structure can be described by genotypic correlation coefficients between groups of individuals, the most basic of which are the pair-wise relatedness coefficients between any two individuals. There are nine pair-wise relatedness coefficients in the most general model, and we show that these can be reduced to seven coefficients for biallelic loci. Although all nine coefficients can be estimated from pedigrees, six coefficients have been beyond empirical reach. We provide a numerical optimization procedure that estimates them from population-genomic data. Simulations show that the procedure is nearly unbiased, even at 3x coverage, and errors in five of the seven coefficients are statistically uncorrelated. The remaining two coefficients have a negative correlation of errors, but their sum provides an unbiased assessment of the overall correlation of heterozygosity between two individuals. Application of these new methods to four populations of the freshwater crustacean Daphnia pulex reveal the occurrence of half-siblings in our samples, as well as a number of identical individuals that are likely obligately asexual clone-mates. Statistically significant negative estimates of these pair-wise relatedness coefficients, including inbreeding coefficents that were typically negative, underscore the difficulties that arise when interpreting genotypic correlations as estimations of the probability that alleles are identical by descent.

Evolutionary Biology↗

bioRxiv2016

Evolution of mating types driven by purifying selection against mitochondrial mutations

Sexual cell fusion combines genetic material of two gametes, but why the two reproductive cells have to belong to distinct self-incompatible gamete classes is not known. In a vast majority of sexual eukaryotes, mitochondria are inherited uniparentally from only one of the two mating types, which is thought to facilitate purifying selection against deleterious mitochondrial mutations and limit the inter-genomic conflicts. Here I argue that two mating types in eukaryotes represent a mechanism of mitochondrial quality control through the highly asymmetric transmission of mitochondrial genes at cell fusion. I develop a mathematical model to explicitly study the evolution of two self-incompatible mating type alleles linked to the nuclear locus controlling the pattern of organelle inheritance. The invasion of mating-type alleles is opposed by the short-term fitness benefit of mitochondrial mixing under negative epistasis and the lower chance of encountering a compatible mating partner. Nevertheless, under high mitochondrial mutation rates purifying selection against defective mitochondria can drive two mating types with uniparental inheritance to fixation. The invasion is further facilitated by the paternal leakage of mitochondria under paternal control of cytoplasmic inheritance. In contrast to previous studies, the model does not rely on the presence of selfish cytoplasmic elements, providing a more universal solution to the longstanding evolutionary puzzle of two sexes.

Evolutionary Biology↗

bioRxiv2016

Sanctions, partner recognition, and variation in mutualistic symbiosis

Mutualistic interactions can be stabilized against invasion by non-cooperative individuals by putting such \"cheaters\" at a selective disadvantage. Selection against cheaters should eliminate genetic variation in partner quality -- yet such variation is often found in natural populations. One explanation for this paradox is that mutualism outcomes are determined not only by responses to partner performance, but also by partner signals. Here, we build a model of coevolution in a symbiotic mutualism, in which hosts ability to sanction non-cooperative symbionts and recognition of symbiont signals are determined by separate loci, as are symbionts cooperation and expression of signals. In the model, variation persists without destabilizing the interaction, in part because coevolution of symbiont signals and host recognition is altered by the coevolution of sanctions and cooperation, and vice-versa. Individual-based simulations incorporating population structure strongly corroborate these results. The dual systems of sanctions and partner recognition converge toward conditions similar to some economic models of mutualistic symbiosis in which hosts offering the right incentives to potential symbionts can initiate symbiosis without screening for partner quality. These results predict that mutualists can maintain variation in recognition of partner signals or in the ability to sanction non-cooperators without destabilizing mutualism, and reinforce the notion that studies of mutualism should consider communication between partners as well as the exchange of benefits.

Evolutionary Biology↗

bioRxiv2016

Inferring node dates from tip dates in fossil Canidae: the importance of tree priors

Tip-dating methods are becoming popular alternatives to traditional node calibration approaches for building time-scaled phylogenetic trees, but questions remain about their application to empirical datasets. We compared the performance of the most popular methods against a dated tree of fossil Canidae derived from previously published monographs. Using a canid morphology dataset, we performed tip-dating using Beast 2.1.3 and MrBayes 3.2.5. We find that for key nodes (Canis, ~3.2 Ma, Caninae ~11.7 Ma) a non-mechanistic model using a uniform tree prior produces estimates that are unrealistically old (27.5, 38.9 Ma). Mechanistic models (incorporating lineage birth, death, and sampling rates) estimate ages that are closely in line with prior research. We provide a discussion of these two families of models (mechanistic vs. non-mechanistic) and their applicability to fossil datasets.

Evolutionary Biology↗

bioRxiv2016

Evolutionary dynamics of chloroplast genomes in low light: a case study of the endolithic green alga Ostreobium quekettii

Some photosynthetic organisms live in extremely low light environments. Light limitation is associated with selective forces as well as reduced exposure to mutagens, and over evolutionary timescales it can leave a footprint on species genome. Here we present the chloroplast genomes of four green algae (Bryopsidales, Ulvophyceae), including the endolithic (limestone-boring) alga Ostreobium quekettii, which is a low light specialist. We use phylogenetic models and comparative genomic tools to investigate whether the chloroplast genome of Ostreobium corresponds to our expectations of how low light would affect genome evolution. Ostreobium has the smallest and most gene-dense chloroplast genome among Ulvophyceae reported to date, matching our expectation that light limitation would impose resource constraints. Rates of molecular evolution are significantly slower along the phylogenetic branch leading to Ostreobium, in agreement with the expected effects of low light and energy levels on molecular evolution. Given the exceptional ability of our model organism to photosynthesize under extreme low light conditions, we expected to observe positive selection in genes related to the photosynthetic machinery. However, we observed stronger purifying selection in these genes, which might either reflect a lack of power to detect episodic positive selection followed by purifying selection and/or a strengthening of purifying selection due to the loss of a gene related to light sensitivity. Besides shedding light on the genome dynamics associated with a low light lifestyle, this study helps to resolve the role of environmental factors in shaping the diversity of genome architectures observed in nature.\n\nData deposition: Chloroplast genome sequences will be deposited in GenBank

Evolutionary Biology↗