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bioRxiv2017

Alzheimer related genes show accelerated evolution

Alzheimer's disease (AD) is a neurodegenerative disorder of unknown cause with complex genetic and environmental traits. Here, we show that gene structures of loci, that show AD-associated changes in their expression, evolve faster than the genome at large. This phylogenetic trait of AD suggests a critical pathogenetic role of recent adaptive evolution of human brain and might have far reaching consequences with respect to the appropriateness of model systems and the development of disease-modifying strategies.

evolutionary biology↗

bioRxiv2017

Evolution and Functional Information

\"Functional Information\"--estimated from the mutual information of protein sequence alignments--has been proposed as a reliable way of estimating the number of proteins with a specified function and the consequent difficulty of evolving a new function. The fantastic rarity of functional proteins computed by this approach emboldens some to argue that evolution is impossible. Random searches, it seems, would have no hope of finding new functions. Here, we use simulations to demonstrate that sequence alignments are a poor estimate functional information. The mutual information of sequence alignments fantastically underestimates of the true number of functional proteins, because it also is strongly influenced by a familys history, mutational bias, and selection. Regardless, even if functional information could be reliably calculated, it tells us nothing about the difficulty of evolving new functions, because it does not estimate the distance between a new function and existing functions. The pervasive observation of multifunctional proteins suggests that functions are actually ver close to one another and abundant. Multifunctional proteins would be impossible if the FI argument against evolution were true.

evolutionary biology↗

bioRxiv2017

Adaptive pathways of coral populations on the Great Barrier Reef

Can genetic adaptation in reef-building corals keep pace with the current rate of sea surface warming? Here we combine population genomic, biophysical modeling, and evolutionary simulations to predict future adaptation of the common coral Acropora millepora on the Great Barrier Reef. Loss of coral cover in recent decades did not yet have detectable effect on genetic diversity in our species. Genomic analysis of migration patterns closely matched the biophysical model of larval dispersal in favoring the spread of existing heat-tolerant alleles from lower to higher latitudes. Given these conditions we find that standing genetic variation could be sufficient to fuel rapid adaptation of A. millepora to warming for the next 100-200 years, although random thermal anomalies would drive increasingly severe mortality episodes. However, this adaptation will inevitably cease unless the warming is slowed down, since no realistic mutation rate could replenish adaptive genetic variation fast enough.

evolutionary biology↗

bioRxiv2017

Can malaria parasites manipulate the odour-mediated host preference of their mosquito vectors?

Malaria parasites can manipulate mosquito feeding behaviours such as motivation and avidity to feed on vertebrate hosts in ways that increase parasite transmission. However, in natural conditions, not all vertebrate blood-sources are suitable hosts for the parasite. Whether malaria parasites can manipulate mosquito host choice in ways that enhance parasite transmission toward suitable hosts and/or reduce mosquito attraction to unsuitable hosts (i.e. specific manipulation) is unknown. To address this question, we experimentally infected three species of mosquito vectors (Anopheles coluzzii, Anopheles gambiae, and Anopheles arabiensis) with wild isolates of the human malaria parasite Plasmodium falciparum, and examined the effects of immature (oocyst) and mature (sporozoite) infections on mosquito behavioural responses (activation rate and odour choice) to combinations of calf odour, human odour and outdoor air using a dual-port olfactometer. Regardless of parasite developmental stage and mosquito species, P. falciparum infection did not alter mosquito activation rate or their choice for human odours. The overall expression pattern of host choice of all three mosquito species was consistent with a high degree of anthropophily, with both infected and uninfected individuals showing higher attraction toward human odour over calf odour, human odour over outdoor air, and outdoor air over calf odour. Our results suggests that, in this system, the parasite may not be able to manipulate the early long-range behavioural steps involved in the mosquito host-feeding process, including initiation of host-seeking and host orientation. Future studies examining mosquito host-feeding behaviours at a shorter range (i.e. the \"at-host\" foraging activities) are required to test whether malaria parasites can modify their mosquito host choice to enhance transmission toward suitable hosts and/or reduce biting on unsuitable hosts.

evolutionary biology↗

bioRxiv2017

The interplay of demography and selection during maize domestication and expansion

The history of maize has been characterized by major demographic events including changes in population size associated with domestication and range expansion as well as gene flow with wild relatives. The interplay between demographic history and selection has shaped diversity across maize populations and genomes. Here, we investigate these processes based on high-depth resequencing data from 31 maize landraces spanning the pre-Columbian distribution of maize as well as four wild progenitor individuals (Zea mays ssp. parviglumis) from the Balsas River Valley in Mexico. Genome-wide demographic analyses reveal that maize domestication and spread resulted in pronounced declines in effective population size due to both a protracted bottleneck and serial founder effects, while, concurrently, parviglumis experienced population growth. The cost of maize domestication and spread was an increase in deleterious alleles in the domesticate relative to its wild progenitor. This cost is particularly pronounced in Andean maize, which appears to have experienced a more dramatic founder event when compared to other maize populations. Introgression from the wild teosinte Zea mays ssp. mexicana into maize in the highlands of Mexico and Guatemala is found found to decrease the prevalence of deleterious alleles, likely due to the higher long-term effective population size of wild maize. These findings underscore the strong interaction between historical demography and the efficiency of selection species- and genome-wide and suggest domesticated species with well-characterized histories may be particularly useful for understanding this interplay.

evolutionary biology↗

bioRxiv2017

Soft sweeps and beyond: Understanding the patterns and probabilities of selection footprints under rapid adaptation

O_LIThe tempo and mode of adaptive evolution determine how natural selection shapes patterns of genetic diversity in DNA polymorphism data. While slow mutation-limited adaptation leads to classical footprints of \"hard\" selective sweeps, these patterns are different when adaptation responds quickly to a novel selection pressure, acting either on standing genetic variation or on recurrent new mutation. In the past decade, corresponding footprints of \"soft\" selective sweeps have been described both in theoretical models and in empirical data.\nC_LIO_LIHere, we summarize the key theoretical concepts and contrast model predictions with observed patterns in Drosophila, humans, and microbes.\nC_LIO_LIEvidence in all cases shows that \"soft\" patterns of rapid adaptation are frequent. However, theory and data also point to a role of complex adaptive histories in rapid evolution.\nC_LIO_LIWhile existing theory allows for important implications on the tempo and mode of the adaptive process, complex footprints observed in data are, as yet, insufficiently covered by models. They call for in-depth empirical study and further model development.\nC_LI

evolutionary biology↗

bioRxiv2017

The genome sizes of ostracod crustaceans correlate with body size and phylogeny

Within animals a positive correlation between genome size and body size has been detected in several taxa but not in others, such that it remains unknown how pervasive this pattern may be. Here we provide another example of a positive relationship, in a group of crustaceans whose genome sizes have not previously been investigated. We analyze genome size estimates for 46 species across Class Ostracoda, including 29 new estimates made using Feulgen image analysis densitometry and flow cytometry. Genome sizes in this group range ~80-fold, a level of variability that is otherwise not seen in crustaceans with the exception of some malacostracan orders. We find a strong positive correlation between genome size and body size across all species, including after phylogenetic correction. We additionally detect evidence of XX/XO sex determination in all three species of myodocopids where male and female genome sizes were estimated. On average, genome sizes are larger but less variable in myodocopids than in podocopids, and marine ostracods have larger genomes than freshwater species, but this appears to be explained by phylogenetic inertia. The relationship between phylogeny, genome size, body size, and habitat is complex in this system, and will benefit from additional data collection across various habitats and ostracod taxa.

evolutionary biology↗

bioRxiv2017

Mutational biases influence parallel adaptation

While mutational biases strongly influence neutral molecular evolution, the role of mutational biases in shaping the course of adaptation is less clear. Here we consider the frequency of transitions relative to transversions among adaptive substitutions. Because mutation rates for transitions are higher than those for transversions, if mutational biases influence the dynamics of adaptation, then transitions should be over-represented among documented adaptive substitutions. To test this hypothesis, we assembled a dataset of putatively adaptive amino acid substitutions that have occurred in parallel during evolution in nature or in the laboratory. We find that the frequency of transitions in this dataset is much higher than would be predicted under a null model where mutation has no effect. Our results are qualitatively similar even if we restrict ourself to changes that have occurred, not merely twice, but three or more times. These results suggest that the course of adaptation is biased by mutation.

evolutionary biology↗

bioRxiv2017

Missing the point (estimate): Bayesian and likelihood phylogenetic reconstructions of morphological characters produce generally concordant inferences. A comment on Puttick et al.

Puttick et al. [1] performed a simulation study to compare accuracy among methods of inferring phylogeny from discrete morphological characters. They report that a Bayesian implementation of the Mk model [2] was most accurate (but with low resolution), while a maximum likelihood (ML) implementation of the same model was least accurate. They conclude by strongly advocating that Bayesian implementations of the Mk model should be the default method of analysis for such data. While we appreciate the authors attempt to investigate the accuracy of alternative methods of analysis, their conclusion is based on an inappropriate comparison of the ML point estimate, which does not consider confidence, with the Bayesian consensus, which incorporates estimation credibility into the summary tree. Using simulation, we demonstrate that ML and Bayesian estimates are concordant when confidence and credibility are comparably reflected in summary trees, a result expected from statistical theory. We therefore disagree with the conclusions of PEA and consider their prescription of any default method to be poorly founded. Instead, we recommend caution and thoughtful consideration of the model or method being applied to a morphological dataset.

evolutionary biology↗

bioRxiv2017

So many genes, so little time: comments on divergence-time estimation in the genomic era

Phylogenomic datasets have been successfully used to address questions involving evolutionary relationships, patterns of genome structure, signatures of selection, and gene and genome duplications. However, despite the recent explosion in genomic and transcriptomic data, the utility of these data sources for efficient divergence-time inference remains unexamined. Phylogenomic datasets pose two distinct problems for divergence-time estimation: (i) the volume of data makes inference of the entire dataset intractable, and (ii) the extent of underlying topological and rate heterogeneity across genes makes model mis-specification a real concern. \"Gene shopping\", wherein a phylogenomic dataset is winnowed to a set of genes with desirable properties, represents an alternative approach that holds promise in alleviating these issues. We implemented an approach for phylogenomic datasets (available in SortaDate) that filters genes by three criteria: (i) clock-likeness, (ii) reasonable tree length (i.e., discernible information content), and (iii) least topological conflict with a focal species tree (presumed to have already been inferred). Such a winnowing procedure ensures that errors associated with model (both clock and topology) mis-specification are minimized, therefore reducing error in divergence-time estimation. We demonstrated the efficacy of this approach through simulation and applied it to published animal (Aves, Diplopoda, and Hymenoptera) and plant (carnivorous Caryophyllales, broad Caryophyllales, and Vitales) phylogenomic datasets. By quantifying rate heterogeneity across both genes and lineages we found that every empirical dataset examined included genes with clock-like, or nearly clock-like, behavior. Moreover, many datasets had genes that were clock-like, exhibited reasonable evolutionary rates, and were mostly compatible with the species tree. We identified overlap in age estimates when analyzing these filtered genes under strict clock and uncorrelated lognormal (UCLN) models. However, this overlap was often due to imprecise estimates from the UCLN model. We find that \"gene shopping\" can be an efficient approach to divergence-time inference for phylogenomic datasets that may otherwise be characterized by extensive gene tree heterogeneity.

evolutionary biology↗

bioRxiv2017

Social interactions within the family enhance the capacity for evolutionary change

Classical models of evolution seldom predict evolution in the wild. One explanation is that the social environment has important, yet overlooked, effects on how traits change in response to natural selection. We tested this idea with selection experiments on burying beetles (Nicrophorus vespilloides), sub-social insects that exhibit biparental care. Populations responded to selection for larger adults only when parents cared for their offspring, and responded to selection for smaller adults only when we prevented parents from providing care. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas conflict can prevent further directional selection.

evolutionary biology↗

bioRxiv2017

Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic radiation of trophic specialist pupfishes

Rapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of the fixed variants between the specialist species lie in regions with discordant topologies. These regions include signatures of selective sweeps and adaptive introgression from neighboring islands into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador contributed 10-fold more to divergence between specialist species within the radiation than adaptive introgression of Caribbean genetic variation; however, some of these introgressed regions from distant islands were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador specialist from an island 300 km away. The complex emerging picture of the origins of adaptive radiation on San Salvador indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may also be required to trigger adaptive radiation in the presence of ecological opportunity.\n\nAuthor summaryGroups of closely related species can rapidly evolve to occupy diverse ecological roles, but the ecological and genetic conditions that trigger this diversification are still highly debated. We examine patterns of molecular evolution across the genomes of a rapid radiation of pupfishes that includes two trophic specialists. Despite apparently widespread ecological opportunities and gene flow across the Caribbean, this radiation is endemic to a single Bahamian Island. Using the whole genomes of 42 pupfish we find evidence of extensive and previously unexpected variation in evolutionary relatedness among Caribbean pupfish. Two sources of genetic variation have contributed to the adaptive diversification of complex phenotypes in this system: selective sweeps of genetic variation from across the Caribbean that was brought into San Salvador through hybridization and genetic variation found on San Salvador. While genetic variation from San Salvador appears to be relatively more common in the divergence observed among specialists, hybridization probably played an important role in the evolution of the complex phenotypes as well. Our findings that multiple sources of genetic variation contribute to the San Salvador radiation suggest that a complex suite of factors, including hybridization with other species, may be required to trigger adaptive radiation in the presence of ecological opportunity.

evolutionary biology↗

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↗