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bioRxiv2016

Evolutionary stability of microbial communities with antibiotic degrading species

A major puzzle in ecology is how antibiotic resistant, sensitive and producer species coexist in close proximity. Recently, we showed that antibiotic degrading species dramatically alter community dynamics: replacing intrinsic resistance with resistance through degradation generates stable communities resilient to spatial mixing, large species abundance perturbations, changes in interaction strengths, and differences in species growth rates. In addition to ecological stability, it is interesting to consider evolutionary stability of these communities to the appearance of cheater species that either cease production or degradation of antibiotics. Our investigation of evolutionary stability of cyclical 3-species communities revealed that these communities are robust to cheaters that stop degrading antibiotics. Our simulations also showed that cheaters that stop producing antibiotics do not take over the community, yet they can transiently invade and cause community collapse. In the analytical approximation we initially investigated, production cheaters with a small fitness advantage can invade the community simply because the benefit of inhibiting competitors is shared among all cells. Here, we consider evolutionary stability to cheaters in our complete model, where spatial mixing is introduced only after a short range colonization step. In this regime, an antibiotic producer cell directly benefits from killing nearby competitor species as it has a greater chance of colonizing the newly voided spaces created by the action of its antibiotic. Simulating response to cheater invasions for the cyclical three species community and for random 4-species ecologically stable topologies, we find that these communities can be fully resilient to both degradation and production cheaters. The strength of selection against cheaters varies with the area of the zone of inhibition around producers and is maximized for weak inhibition, where there is less overlap between the killing zones of neighboring cells. These results may aid the construction of complex synthetic communities that are both ecological and evolutionary stable.

Evolutionary Biology↗

bioRxiv2016

Are sexually selected traits affected by a poor environment early in life?

Conditions experienced early in life can affect key life-history traits. Individuals that experience a poor nutritional environment early in life can reduce potential costs by delaying sexual maturation. The direct costs of delaying maturation are well known (i.e. delayed onset of breeding), but individuals can also face additional costs as adults. Some of these hidden costs accrue due to cryptic morphological and physiological changes. In mosquitofish (Gambusia holbrooki), males with limited food intake early in life delay maturation to eventually reach a similar adult body size to their well-fed counterparts ( catch-up growth). Here we tested whether a poor diet early in life incurs hidden costs due to reduced expression of sexually selected male traits (genital size and ejaculate traits). We found that diet early in life significantly influenced sperm reserves and replenishment rate due to age and development-rate dependent effects. Although catching-up in body size ameliorates some of the costs of a poor start in life for males, our findings suggest that long-term fitness costs might arise because of sexually selection against these males. Our results highlight that fitness costs of a poor start in life can extend into adulthood.

Evolutionary Biology↗

bioRxiv2016

Mixing of Porpoise Ecotypes in South Western UK Waters Revealed by Genetic Profiling

Contact zones between marine ecotypes are of interest for understanding how key pelagic predators may react to climate change. We analysed the fine scale genetic structure and morphological variation in harbour porpoises around the UK, at the proposed northern limit of a contact zone between southern and northern ecotypes in the Bay of Biscay. Using a sample of 591 stranded animals spanning a decade and microsatellite profiling at 9 loci, clustering and spatial analyses revealed that animals stranded around UK are composed of mixed genetic ancestries from two genetic pools. Porpoises from SW England displayed a distinct genetic ancestry, had larger body-sizes and inhabit an environment differentiated from other UK costal areas. Genetic ancestry blends from one group to the other along a SW-NE axis along the UK coastline, and showed a significant association with body size, consistent with morphological differences between the two ecotypes and their mixing around the SW coast. We also found significant isolation-by-distance among juveniles, suggesting that stranded juveniles display reduced intergenerational dispersal, while adults show larger variance. The fine scale structure of this admixture zone raises the question of how it will respond to future climate change and provides a reference point for further study.

Evolutionary Biology↗

bioRxiv2016

Evolutionary determinants of morphological polymorphism in colonial animals

Colonial animals commonly exhibit morphologically polymorphic modular units that are phenotypically distinct and specialize in specific functional tasks. But how and why these polymorphic modules have evolved is poorly understood. Across colonial invertebrates there is wide variation in the degree of polymorphism from none in colonial ascidians, to extreme polymorphism in siphonophores such as the Portuguese Man of War. Bryozoa are a phylum of exclusively colonial invertebrates that uniquely exhibit almost the entire range of polymorphism from monomorphic species to others that rival siphonophores in their polymorphic complexity. Previous approaches to understanding the evolution of polymorphism have been based upon analyses of (1) the functional role of polymorphs or (2) presumed evolutionary costs and benefits based upon evolutionary theory that postulates polymorphism should only be evolutionarily sustainable in more \"stable\" environments because polymorphism commonly leads to the loss of feeding and sexual competence. Here we use bryozoans from opposite shores of the Isthmus of Panama to revisit the environmental hypothesis by comparison of faunas from distinct oceanographic provinces that differ greatly in environmental variability and we then examine the correlations between the extent of polymorphism in relation to patterns of ecological succession and variation in life histories. We find no support for the environmental hypothesis. Distributions of the incidence of polymorphism in the oceanographically unstable Eastern Pacific are indistinguishable from those in the more stable Caribbean. In contrast, the temporal position of species in a successional sequence is collinear with the degree of polymorphism because species with fewer types of polymorphs are competitively replaced by species with higher numbers of polymorphs on the same substrata. Competitively dominant species also exhibit patterns of growth that increase their competitive ability. The association between degrees of polymorphism and variations in life histories is fundamental to understanding of the macroevolution of polymorphism.

Evolutionary Biology↗

bioRxiv2016

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization in Drosophila

Argonaute2 (Ago2) is a rapidly evolving nuclease in the Drosophila melanogaster RNA interference (RNAi) pathway that targets viruses and transposable elements in somatic tissues. Here we reconstruct the history of Ago2 duplications across the Drosophila obscura group, and use patterns of gene expression to infer new functional specialization. We show that some duplications are old, shared by the entire species group, and that losses may be common, including previously undetected losses in the lineage leading to D. pseudoobscura. We find that while the original (syntenic) gene copy has generally retained the ancestral ubiquitous expression pattern, most of the novel Ago2 paralogues have independently specialized to testis-specific expression. Using population genetic analyses, we show that most testis-specific paralogues have significantly lower genetic diversity than the genome-wide average. This suggests recent positive selection in three different species, and model-based analyses provide strong evidence of recent hard selective sweeps in or near four of the six D. pseudoobscura Ago2 paralogues. We speculate that the repeated evolution of testis-specificity in obscura group Ago2 genes, combined with their dynamic turnover and strong signatures of adaptive evolution, may be associated with highly derived roles in the suppression of transposable elements or meiotic drive. Our study highlights the lability of RNAi pathways, even within well-studied groups such as Drosophila, and suggests that strong selection may act quickly after duplication in RNAi pathways, potentially giving rise to new and unknown RNAi functions in non-model species.\n\nSupporting DataAll new sequences produced in this study have been submitted to Genbank as KX016642-KX016771.

Evolutionary Biology↗

bioRxiv2016

The evolution of mutual mate choice under direct benefits

In nature, the intensity of mate choice (i.e., choosiness) is highly variable within and between sexes. Despite growing empirical evidence showing male and/or mutual mate choice, theoretical investigations of the joint evolution of female and male choosiness are few. In addition, previous approaches have often assumed an absence of trade-off between the direct benefits per mating and the lower mating rate that results from being choosy. Here, we model the joint evolution of female and male choosiness when it is solely ruled by this fundamental trade-off. We show that this trade-off can generate a diversity of stable combinations of choosiness. Mutual mate choice can only evolve if both females and males exhibit long latency after mating. Further, we show that an increase in choosiness in one sex does not necessarily prevent the evolution of mutual mate choice: the outcome depends on details of the life history, the decision rule for mate choice, and how the fecundity of a pair is shaped by the quality of both individuals. Lastly, we discuss the power of the sensitivity of the relative searching time (i.e., of the proportion of lifetime spent searching for mates) as a predictor of the joint evolution of choosiness.

Evolutionary Biology↗

bioRxiv2016

The CARD-CC/Bcl10/paracaspase signaling complex is functionally conserved since the last common ancestor of planulozoa.

Type 1 paracaspases originated in the Ediacaran geological period before the last common ancestor of bilaterians and cnidarians (Planulozoa). Cnidarians have several paralog type 1 paracaspases, type 2 paracaspases, and a homolog of Bcl10. Notably in bilaterians, lineages like nematodes and insects lack Bcl10 whereas other lineages such as vertebrates, hemichordates, annelids and mollusks have a Bcl10 homolog. A survey of invertebrate CARD-coiled-coil (CC) domain homologs of CARMA/CARD9 revealed such homologs only in species with Bcl10, indicating an ancient co-evolution of the entire CARD-CC/Bcl10/MALT1-like paracaspase (CBM) complex. Furthermore, vertebrate-like Syk/Zap70 tyrosine kinase homologs with the ITAM-binding SH2 domain were found in invertebrate organisms with CARD-CC/Bcl10, indicating that this pathway might be the original user of the CBM complex. We also established that the downstream signaling proteins TRAF2 and TRAF6 are functionally conserved in Cnidaria. There also seems to be a correlation where invertebrates with CARD-CC and Bcl10 have type 1 paracaspases which are more similar to the paracaspases found in vertebrates. A proposed evolutionary scenario includes at least two ancestral type 1 paracaspase paralogs in the planulozoan last common ancestor, where at least one paralog usually is dependent on CARD-CC/Bcl10 for its function. Functional analyses of invertebrate type 1 paracaspases and Bcl10 homologs support this scenario and indicate an ancient origin of the CARD-CC/Bcl10/paracaspase signaling complex. Results from cnidarians, nematodes and mice also suggest an ancient neuronal role for the type 1 paracaspases.

Evolutionary Biology↗

bioRxiv2016

Potential pitfalls in estimating viral load heritability

In HIV patients, the set-point viral load (SPVL) is the most widely used predictor of disease severity. Yet SPVL varies over several orders of magnitude between patients. The heritability of SPVL quantifies how much of the variation in SPVL is due to transmissible viral genetics. There is currently no clear consensus on the value of SPVL heritability, as multiple studies have reported apparently discrepant estimates. Here we illustrate that the discrepancies in estimates are most likely due to differences in the estimation methods, rather than the study populations. Importantly, phylogenetic estimates run the risk of being strongly confounded by unrealistic model assumptions. Care must be taken when interpreting and comparing the different estimates to each other.

Evolutionary Biology↗

bioRxiv2016

Peculiar hybrid genomes of devastating plant pests promote plasticity in the absence of sex and meiosis

Root-knot nematodes (genus Meloidogyne) show an intriguing diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most damaging species to the world agriculture are those that reproduce without meiosis and without sex. To understand this parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of 3 obligatory ameiotic asexual Meloidogyne species and have compared them to those of meiotic relatives with facultative or obligatory asexual reproduction. Our comparative genomic analysis shows that obligatory asexual root-knot nematodes have a higher abundance of transposable elements (TE) compared to the facultative sexual and contain duplicated regions with a high within-species average nucleotide divergence of 8%. Phylogenomic analysis of the genes present in these duplicated regions suggests that they originated from multiple hybridization events. The average nucleotide divergence in the coding portions between duplicated regions is ~5-6 % and we detected diversifying selection between the corresponding gene copies. Genes under diversifying selection covered a wide spectrum of predicted functional categories which suggests a high impact of the genome structure at the functional level. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, suggesting that these putative hybrids share a recent common maternal donor lineage. The intriguing parasitic success of mitotic root-knot nematodes in the absence of sex may be partly explained by TE-rich composite genomes resulting from multiple allo-polyploidization events and promoting plasticity in the absence of sex.

Evolutionary Biology↗

bioRxiv2016

Lethal Gene Drive Selects Inbreeding

The use of selfish gene drive systems to suppress or even extinguish populations has been proposed on theoretical grounds for almost half a century. Creating these genes has recently become possible with CRISPR technology. One seemingly feasible approach, originally proposed by Burt, is to create a homing endonuclease gene (HEG) that inserts into an essential gene, enabling heterozygote viability but causing homozygote lethality. With 100% segregation distortion in gametes, such genes can cause profound population suppression if resistance does not evolve. Here, population genetic models are used to consider the evolution of inbreeding (specifically selfing) as a possible response to a recessively lethal HEG with complete segregation distortion. Numerical analyses indicate a rich set of outcomes, but selfing often evolves in response to the HEG, with a corresponding partial restoration of mean fitness. Whether selfing does indeed evolve and its effect in restoring fitness depends heavily on the magnitude of inbreeding depression. Overall, these results point toward an underappreciated evolutionary response to block the harmful effects of a selfish gene. They raise the possibility that extreme population suppression may be more difficult to achieve than currently imagined.

Evolutionary Biology↗

bioRxiv2016

Effects of linked selective sweeps on demographic inference and model selection

The availability of large-scale population genomic sequence data has resulted in an explosion in efforts to infer the demographic histories of natural populations across a broad range of organisms. As demographic events alter coalescent genealogies they leave detectable signatures in patterns of genetic variation within and between populations. Accordingly, a variety of approaches have been designed to leverage population genetic data to uncover the footprints of demographic change in the genome. The vast majority of these methods make the simplifying assumption that the measures of genetic variation used as their input are unaffected by natural selection. However, natural selection can dramatically skew patterns of variation not only at selected sites, but at linked, neutral loci as well. Here we assess the impact of recent positive selection on demographic inference by characterizing the performance of three popular methods through extensive simulation of datasets with varying numbers of linked selective sweeps. In particular, we examined three different demographic models relevant to a number of species, finding that positive selection can bias parameter estimates of each of these models--often severely. Moreover, we find that selection can lead to incorrect inferences of population size changes when none have occurred. We argue that the amount of recent positive selection required to skew inferences may often be acting in natural populations. These results suggest that demographic studies conducted in many species to date may have exaggerated the extent and frequency of population size changes.

Evolutionary Biology↗

bioRxiv2016

The promise of disease gene discovery in South Asia

The more than 1.5 billion people who live in South Asia are correctly viewed not as a single large population, but as many small endogamous groups. We assembled genome-wide data from over 2,800 individuals from over 260 distinct South Asian groups. We identify 81 unique groups, of which 14 have estimated census sizes of more than a million, that descend from founder events more extreme than those in Ashkenazi Jews and Finns, both of which have high rates of recessive disease due to founder events. We identify multiple examples of recessive diseases in South Asia that are the result of such founder events. This study highlights an under-appreciated opportunity for reducing disease burden among South Asians through the discovery of and testing for recessive disease genes.

Evolutionary Biology↗

bioRxiv2016

An evolutionary medicine perspective on Neandertal extinction

The Eurasian sympatry of Neandertals and anatomically modern humans - beginning at least 45,000 years ago and lasting for more than 5,000 years - has long sparked anthropological interest into the factors that potentially contributed to Neandertal extinction. Among many different hypotheses, the \"differential pathogen resistance\" extinction model posits that Neandertals were disproportionately affected by exposure to novel infectious diseases that were transmitted during the period of spatiotemporal sympatry with modern humans. Comparisons of new archaic hominin paleogenome sequences with modern human genomes have confirmed a history of genetic admixture - and thus direct contact - between humans and Neandertals. Analyses of these data have also shown that Neandertal nuclear genome genetic diversity was likely considerably lower than that of the Eurasian anatomically modern humans with whom they came into contact, perhaps leaving Neandertal innate immune systems relatively more susceptible to novel pathogens. In this study, we compared levels of genetic diversity in genes for which genetic variation is hypothesized to benefit pathogen defense among Neandertals and African, European, and Asian modern humans, using available exome sequencing data (six chromosomes per population). We observed that Neandertals had only 31-39% as many nonsynonymous (amino acid changing) polymorphisms across 73 innate immune system genes compared to modern human populations. We also found that Neandertal genetic diversity was relatively low in an unbiased set of balancing selection candidate genes for primates - genes with the highest 1% genetic diversity genome-wide in non-human apes. In contrast, Neandertals had similar to higher levels of genetic diversity than humans in 13 major histocompatibility complex (MHC) genes. Thus, while Neandertals may have been relatively more susceptible to some novel pathogens and differential pathogen resistance could be considered as one potential contributing factor in their extinction, this model does have limitations.

Evolutionary Biology↗

bioRxiv2016

Genome-wide evidence for a hybrid origin of modern polar bears

Interspecific hybridization is recognized as a widespread phenomenon but measuring its extent, directionality, and adaptive importance in the evolution of species remain challenging. Polar bears possess unique adaptations to life on the Arctic sea ice, whereas their closest relatives -brown bears - are boreal and subarctic generalists. Despite largely non-overlapping modern distributions, genomic evidence demonstrates ancient admixture between these species. Here, we analyze new genomes from contemporary zones of species overlap as well as a previously sequenced 120,000-year old polar bear subfossil. We use explicit statistical fitting of data to admixture graphs to provide a framework for testing alternative scenarios of population relationships and gene flow directionality. Our analyses favor a single, parsimonious introgression event from relatives of extant Southeast Alaskan coastal brown bears into the ancestor of extant polar bears, which inverts the current paradigm of unidirectional gene flow from polar into brown bear. This conclusion has clear implications for our understanding of the impact of climate change: a specialist Arctic lineage may have been the recipient of generalist, boreal genetic variants at crucial times during critical phases of Northern Hemisphere glacial oscillations.

Evolutionary Biology↗

bioRxiv2016

Why Mutant Allele Frequencies in Oncogenes Peak Around 0.40 and Rapidly Decrease?

The mutant allele frequencies in oncogenes peak around 0.40 and rapidly decrease. In this article, we explain why this is the case. Invoking a key result from mathematical analysis in our model, namely, the inverse function theorem, we estimate the selection pressures of the mutations as a function of germline allele frequencies. Under complete dominance of oncogenic mutations, this selection function is expected to be linearly correlated with the distribution of the mutant alleles. We demonstrate that this is the case by investigating the allele frequencies of mutations in oncogenes across various cancer types, validating our model for mean effective selection. Consistent with the population genetics model of fitness, the selection function fits a gamma distribution curve that accurately describes the trend of the mutant allele frequencies. While existing equations for selection explain evolution at low allele frequencies, our equations are general formulas for natural selection under complete dominance operating at all frequencies. We show that selection exhibits linear behavior at all times, favoring dominant alleles with respect to the change in recessive allele frequency. Also, these equations show, selection behaves like power-law against the recessive alleles at low dominant allele frequency.

Evolutionary Biology↗

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↗