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bioRxiv2015

Evaluating the performance of selection scans to detect selective sweeps in domestic dogs

Selective breeding of dogs has resulted in repeated artificial selection on breed-specific morphological phenotypes. A number of quantitative trait loci associated with these phenotypes have been identified in genetic mapping studies. We analyzed the population genomic signatures observed around the causal mutations for 12 of these loci in 25 dog breeds, for which we genotyped 25 individuals in each breed. By measuring the population frequencies of the causal mutations in each breed, we identified those breeds in which specific mutations most likely experienced positive selection. These instances were then used as positive controls for assessing the performance of popular statistics to detect selection from population genomic data. We found that artificial selection during dog domestication has left characteristic signatures in the haplotype and nucleotide polymorphism patterns around selected loci that can be detected in the genotype data from a single population sample. However, the sensitivity and accuracy at which such signatures were detected varied widely between loci, the particular statistic used, and the choice of analysis parameters. We observed examples of both hard and soft selective sweeps and detected strong selective events that removed genetic diversity almost entirely over regions >10 Mbp. Our study demonstrates the power and limitations of selection scans in populations with high levels of linkage disequilibrium due to severe founder effects and recent population bottlenecks.

Evolutionary Biology↗

bioRxiv2015

A segregating inversion generates fitness variation in a yellow monkeyflower (Mimulus guttatus) population

Polymorphic chromosomal rearrangements, which can bind together hundreds of genes into single genetic loci with diverse effects, are increasingly associated with local adaptation and speciation. They may also be an important component of genetic variation within populations. We genetically and phenotypically characterized a novel segregating inversion (inv6) in the Iron Mountain (IM) population of Mimulus guttatus (yellow monkeyflower). We first identified a region of recombination suppression in three F2 mapping populations resulting from crosses among IM plants; in each case, the F1 hybrid parent was heterozygous for a homogenous derived haplotype (inv6) across markers spanning over 4.2 Mb of Linkage Group 6. Genotype-phenotype associations in the three F2 populations demonstrated negative inv6 effects on male and female fitness components. In addition, inv6 carriers suffered a ~30% loss of pollen viability in the field. Despite these costs, inv6 exists at moderate and apparently stable frequency (~7%) in the natural population, suggesting counter-balancing fitness benefits that maintain the polymorphism. Across four years of monitoring in the field, inv6 had an overall significant positive effect on the seed production (lifetime female fitness) of carriers. This benefit was particularly strong in harsh years and may be mediated (in part) by strong positive inv6 effects on flower production. These data suggest that opposing fitness effects maintain an intermediate frequency, and as a consequence, inv6 generates inbreeding depression and high genetic variance. We discuss these findings in the context of theory about the genetic basis of inbreeding depression and the role for chromosomal rearrangements in population divergence with gene flow.

Evolutionary Biology↗

bioRxiv2015

Biogeographic dating of speciation times using paleogeographically informed processes

Standard models of molecular evolution cannot estimate absolute speciation times alone, and require external calibrations to do so. Because fossil calibration methods rely on the unreliable fossil record, most nodes in the tree of life are dated with poor accuracy. However, many major paleogeographical events are dated, and since biogeographic processes depend on paleogeographical conditions, biogeographic dating may be used as an alternative or complementary method to fossil dating. I demonstrate how a time-stratified biogeographic stochastic process may be used to estimate absolute divergence times by conditioning on dated paleogeographical events. Informed by the current paleogeographical literature, I construct an empirical dispersal graph using 25 areas and 26 epochs for the past 540 Ma of Earths history. Simulations indicate biogeographic dating performs well so long as paleogeography imposes constraint on biogeographic character evolution. To gauge whether biogeographic dating may have any practical use, I analyze the well-studied turtle clade (Testudines) then assess how well biogeographic dating fares compared to heavily fossil-calibrated dating results as reported in the literature. Fossil-free biogeographic dating estimated the age of the most recent common ancestor of extant turtles to be approximately 201 Ma, which is consistent with fossil-based estimates. Accuracy improves further when including a root node fossil calibration. The described model, paleogeographical dispersal graph, and analysis scripts are available for use with RevBayes.

Evolutionary Biology↗

bioRxiv2015

Trees, Population Structure, F-statistics!

Many questions about human genetic history can be addressed by examining the patterns of shared genetic variation between sets of populations. A useful methodological framework for this purpose are F-statistics, that measure shared genetic drift between sets of two, three and four populations, and can be used to test simple and complex hypotheses about admixture between populations. Here, we put these statistics in context of phylogenetic and population genetic theory. We show how measures of genetic drift can be interpreted as branch lengths, paths through an admixture graph or in terms of the internal branches in coalescent trees. We show that the admixture tests can be interpreted as testing general properties of phylogenies, allowing us to generalize applications for arbitrary phylogenetic trees. Furthermore, we derive novel expressions for the F-statistics, which enables us to explore the behavior of F-statistic under population structure models. In particular, we show that population substructure may complicate inference.\n\nAuthor SummaryFor the analysis of genetic data from hundreds of populations, a commonly used technique are a set of simple statistics on data from two, three and four populations. These statistics are used to test hypotheses involving the history of populations, in particular whether data is consistent with the history of a set of populations forming a tree.\n\nHere, we provide context to these statistics by deriving novel expressions and by relating them to approaches in comparative phylogenetics. These results are useful because they provide a straightforward interpretation of these statistics under many demographic processes and lead to simplified expressions. However, the result also reveals the limitations of F-statistics, in that population substructure may complicate inference.

Evolutionary Biology↗

bioRxiv2015

Dietary Breadth is Positively Correlated with Venom Complexity in Cone Snails

Although diet is believed to be a major factor underlying the evolution of venom, few comparative studies examine both venom composition and diet across a radiation of venomous species. Cone snails within the family, Conidae, comprise more than 700 species of carnivorous marine snails that capture their prey by using a cocktail of venomous neurotoxins (conotoxins or conopeptides). Venom composition across species has been previously hypothesized to be shaped by (a) prey taxonomic class (i.e., worms, molluscs, or fish) and (b) dietary breadth. We tested these hypotheses under a comparative phylogenetic framework using ecological data in conjunction with venom duct transcriptomes sequenced from 12 phylogenetically disparate cone snail species, including 10 vermivores (worm-eating), one molluscivore, and one generalist. We discovered 2223 unique conotoxin precursor peptides that encoded 1864 unique mature toxins across all species, >90% of which are new to this study. In addition, we identified two novel gene superfamilies and 16 novel cysteine frameworks. Each species exhibited unique venom profiles, with venom composition and expression patterns among species dominated by a restricted set of gene superfamilies and mature toxins. In contrast with the dominant paradigm for interpreting Conidae venom evolution, prey taxonomic class did not predict venom composition patterns among species. Our results suggests that cone snails have either evolved species-specific expression patterns likely as a consequence of the rapid evolution of conotoxin genes, or that traditional means of categorizing prey type (i.e., worms, mollusc, or fish) and conotoxins (i.e., by gene superfamily) do not accurately encapsulate evolutionary dynamics between diet and venom composition. We also found a significant positive relationship between dietary breadth and measures of conotoxin complexity. These results indicate that species with more generalized diets tend to have more complex venoms and utilize a greater number of venom genes for prey capture. Whether this increased gene diversity confers an increased capacity for evolutionary change remains to be tested. Overall, our results corroborate the key role of diet in influencing patterns of venom evolution in cone snails and other venomous radiations.

Evolutionary Biology↗

bioRxiv2015

Phylogenomic Reconstruction Supports Supercontinent Origins for Leishmania

Leishmania, a genus of parasites transmitted to human hosts and mammalian/reptilian reservoirs by an insect vector, is the causative agent of the human disease complex leishmaniasis. The evolutionary relationships within the genus Leishmania and its origins are the source of ongoing debate, reflected in conflicting phylogenetic and biogeographic reconstructions. This study employs a recently described bioinformatics method, SISRS, to identify over 200,000 informative sites across the genome from newly sequenced and publicly available Leishmania data. This dataset is used to reconstruct the evolutionary relationships of this genus. Additionally, we constructed a large multi-gene dataset; we used this dataset to reconstruct the phylogeny and estimate divergence dates for species. We conclude that the genus Leishmania evolved at least 90-100 million years ago. Our results support the hypothesis that Leishmania clades separated prior to, and during, the breakup of Gondwana. Additionally, we confirm that reptile-infecting Leishmania are derived from mammalian forms, and that the species that infect porcupines and sloths form a clade long separated from other species. We also firmly place the guinea-pig infecting species, L. enrietti, the globally dispersed L. siamensis, and the newly identified Australia species from kangaroos as sibling species whose distribution arises from the ancient connection between Australia, Antarctica, and South America.

Evolutionary Biology↗

bioRxiv2015

Gene Regulatory Evolution During Speciation in a Songbird

Over the last decade tremendous progress has been made towards a comparative understanding of gene regulatory evolution. However, we know little about how gene regulation evolves in birds, and how divergent genomes interact in their hybrids. Because of unique features of birds - female heterogamety, a highly conserved karyotype, and the slow evolution of reproductive incompatibilities - an understanding of regulatory evolution in birds is critical to a comprehensive understanding of regulatory evolution and its implications for speciation. Using a novel complement of analyses of replicated RNA-seq libraries, we demonstrate abundant divergence in gene expression between subspecies of zebra finches Taeniopygia guttata. By comparing parental populations and their F1 hybrids, we also show that gene misexpression is relatively rare, a pattern that may partially explain the slow buildup of postzygotic reproductive isolation observed in birds relative to other taxa. Although we expected that the action of genetic drift on the island-dwelling zebra finch subspecies would be manifested in a high rate of trans regulatory divergence, we found that most divergence was in cis regulation, following a pattern commonly observed in other taxa. Thus our study highlights both unique and shared features of avian regulatory evolution.

Evolutionary Biology↗

bioRxiv2015

Sex and Ageing: The Role of Sexual Recombination in Longevity

1I use a set of machines based on the concept of nested rule systems built on the a modified version of the Wolfram elemental cellular automata to investigate the role of recombination in providing resistance to ageing. Class III and class IV machines are observed to respond differently to recombination. Class IV machines show recombinational centring in their neutral networks whereas class III machines respond negatively to recombination. Rule 110 shows a unusual response to recombination. Recombination selects for resistance to recombination, the population moves to regions of genome space with high redundancy, this results in organisms with highly robust genomes, more likely to complete development and to be long lived. The increase in longevity may be sufficient to compensate for the costs of sex, including the two fold cost of sex, through increased reproductive potential in long lived organisms requiring long maturation times. Large complex species should therefore be resistant to invasion by asexual mutants whereas small simple organisms with early maturation should be vulnerable to invasion by asexual forms.

Evolutionary Biology↗

bioRxiv2015

Dissecting the genetic basis of a complex cis-regulatory adaptation

Although single genes underlying several evolutionary adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. Here we report that the budding yeast Saccharomyces paradoxus has recently evolved resistance to citrinin, a naturally occurring mycotoxin. Applying a genome-wide test for selection on cis-regulation, we identified five genes involved in the citrinin response that are constitutively up-regulated in S. paradoxus. Four of these genes are necessary for resistance, and are also sufficient to increase the resistance of a sensitive strain when over-expressed. Moreover, cis-regulatory divergence in the promoters of these genes contributes to resistance, while exacting a cost in the absence of citrinin. Our results demonstrate how the subtle effects of individual regulatory elements can be combined, via natural selection, into a complex adaptation. Our approach can be applied to dissect the genetic basis of polygenic adaptations in a wide range of species.\n\nAuthor SummaryAdaptation via natural selection has been a subject of great interest for well over a century, yet we still have little understanding of its molecular basis. What are the genetic changes that are actually being selected? While single genes underlying several adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. The complex trait that we study here is the resistance of Saccharomyces yeast to a mycotoxin called citrinin, which is produced by many other species of fungi, and is a common food contaminant for both humans and livestock. We found that sequence changes in the promoters of at least three genes have contributed to citrinin resistance, by up-regulating their transcription even in the absence of citrinin. Higher expression of these genes confers a fitness advantage in the presence of citrinin, while exacting a cost in its absence-- a fitness tradeoff. Our results provide a detailed view of a complex adaptation, and our approach can be applied to polygenic adaptations in a wide range of species.

Evolutionary Biology↗

bioRxiv2015

Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and M. nudatus

O_LIDivergence of developmental mechanisms within populations may lead to hybrid developmental failure, and may be a factor driving speciation in angiosperms.\nC_LIO_LIWe investigate patterns of endosperm and embryo development in Mimulus guttatus and the closely related, serpentine endemic M. nudatus, and compare them to those of reciprocal hybrid seed. We address whether disruption in hybrid seed development is the primary source of reproductive isolation between these sympatric taxa.\nC_LIO_LIM. guttatus and M. nudatus differ in the pattern and timing of endosperm and embryo development. Some hybrid seed exhibit early disruption of endosperm development and are completely inviable, while others develop relatively normally at first, but later exhibit impaired endosperm proliferation and low germination success. These developmental patterns are reflected in mature hybrid seed, which are either small and flat (indicating little to no endosperm), or shriveled (indicating reduced endosperm volume). Hybrid seed inviability forms a potent reproductive barrier between M. guttatus and M. nudatus.\nC_LIO_LIWe shed light on the extent of developmental variation between closely related species within the M. guttatus species complex, an important ecological model system, and provide a partial mechanism for the hybrid barrier between M. guttatus and M. nudatus.\nC_LI

Evolutionary Biology↗

bioRxiv2015

Evolution of increased larval competitive ability in Drosophila melanogaster without increased larval feeding rate

Multiple experimental evolution studies on D. melanogaster in the 1980s and 1990s indicated that enhanced competitive ability evolved primarily through increased larval tolerance to nitrogenous wastes and increased larval feeding and foraging rate, at the cost of efficiency of food conversion to biomass, and this became the widely accepted view of how adaptation to larval crowding evolves in fruitflies. We recently showed that populations of D. ananassae and D. n. nasuta subjected to extreme larval crowding evolved greater competitive ability without evolving higher feeding rates, primarily through a combination of reduced larval duration, faster attainment of minimum critical size for pupation, greater efficiency of food conversion to biomass, increased pupation height and, perhaps, greater urea/ammonia tolerance. This was a very different suite of traits than that seen to evolve under similar selection in D. melanogaster and was closer to the expectations from the theory of K-selection. At that time, we suggested two possible reasons for the differences in the phenotypic correlates of greater competitive ability seen in the studies with D. melanogaster and the other two species. First, that D. ananassae and D. n. nasuta had a very different genetic architecture of traits affecting competitive ability compared to the long-term, laboratory populations of D. melanogaster used in the earlier studies, either because the populations of the former two species were relatively recently wild-caught, or by virtue of being different species. Second, that the different evolutionary trajectories in D. ananassae and D. n. nasuta versus D. melanogaster were a reflection of differences in the manner in which larval crowding was imposed in the two sets of selection experiments. The D. melanogaster studies used a higher absolute density of eggs per unit volume of food, and a substantially larger total volume of food, than the studies on D. ananassae and D. n. nasuta. Here, we show that long-term laboratory populations of D. melanogaster, descended from some of the populations used in the earlier studies, evolve essentially the same set of traits as the D. ananassae and D. n. nasuta crowding-adapted populations when subjected to a similar larval density at low absolute volumes of food. As in the case of D. ananassae and D. n. nasuta, and in stark contrast to earlier studies with D. melanogaster, these crowding-adapted populations of D. melanogaster did not evolve greater larval feeding rates as a correlate of increased competitive ability. The present results clearly suggest that the suite of phenotypes through which the evolution of greater competitive ability is achieved in fruitflies depends critically not just on larval density per unit volume of food, but also on the total amount of food available in the culture vials. We discuss these results in the context of an hypothesis about how larval density and the height of the food column in culture vials might interact to alter the fitness costs and benefits of increased larval feeding rates, thus resulting in different routes to the evolution of greater competitive ability, depending on the details of exactly how the larval crowding was implemented.

Evolutionary Biology↗

bioRxiv2015

Viruses are a dominant driver of protein adaptation in mammals

Viruses interact with hundreds to thousands of proteins in mammals, yet adaptation against viruses has only been studied in a few proteins specialized in antiviral defense. Whether adaptation to viruses typically involves only specialized antiviral proteins or affects a broad array of proteins is unknown. Here, we analyze adaptation in ~1,300 virus-interacting proteins manually curated from a set of 9,900 proteins conserved across mammals. We show that viruses (i) use the more evolutionarily constrained proteins from the cellular functions they hijack and that (ii) despite this high constraint, virus-interacting proteins account for a high proportion of all protein adaptation in humans and other mammals. Adaptation is elevated in virus-interacting proteins across all functional categories, including both immune and non-immune functions. Our results demonstrate that viruses are one of the most dominant drivers of evolutionary change across mammalian and human proteomes.

Evolutionary Biology↗

bioRxiv2015

Enhancement of larval immune system traits as a correlated response to selection for rapid development in Drosophila melanogaster

We have shown earlier that the evolution of rapid development is accompanied by a correlated decrease in larval feeding rate and competitive ability in laboratory populations of Drosophila melanogaster (Prasad et al. 2001; Shakarad et al. 2005). Here, we show that our faster developing populations have evolved higher hemocyte density and phenol oxidase activity in the larval hemolymph. The increased hemocyte density could be responsible for the evolution of decreased feeding rate as hemocytes and the cephalopharyngeal musculature share common embryonic precursor cells (Kraajiveld et al. 2001). We also show that the bacterial load in larval food vials of the faster developing populations is substantially higher than in controls. Our results suggest that the evolution of reduced competitive ability in the faster developing populations is probably due to larval feeding rate trading off with enhanced larval immune system function. Enhanced larval immune function, in turn, is most likely selected for due to the role of hemocytes (Lanot et al. 2001, Wood and Jacinto 2007) and phenol oxidase (Pentz et al. 1986) in development, and perhaps also due to inadvertent selection on immune performance resulting from the higher bacterial load faced by larvae in the faster developing populations.

Evolutionary Biology↗

bioRxiv2015

Modes of migration and multilevel selection in evolutionary multiplayer games

The evolution of cooperation in group-structured populations has received much attention, but little is known about the effects of different modes of migration of individuals between groups. Here, we have incorporated four different modes of migration that differ in the degree of coordination among the individuals. For each mode of migration, we identify the set of multiplayer games in which the cooperative strategy has higher fixation probability than defection. The comparison shows that the set of games under which cooperation may evolve generally expands depending upon the degree of coordination among the migrating individuals. Weak altruism can evolve under all modes of individual migration, provided that the benefit to cost ratio is high enough. Strong altruism, however, evolves only if the mode of migration involves coordination of individual actions. Depending upon the migration frequency and degree of coordination among individuals, conditions that allow selection to work at the level of groups can be established.

Evolutionary Biology↗

bioRxiv2015

Inferring the correlated fitness effects of nonsynonymous mutations at the same site using triallelic population genomics

The distribution of mutation fitness effects is central to evolutionary genetics. Typical univariate distributions, however, cannot model the effects of multiple mutations at the same site, so we introduce a model in which mutations at the same site have correlated fitness effects. To infer the strength of that correlation, we developed a diffusion approximation to the triallelic frequency spectrum, which we applied to data from D. melanogaster. We found a moderate correlation between the fitness effects of nonsynonymous mutations at the same codon, suggesting that both mutation identity and location are important for determining fitness effects in proteins. We validated our approach by comparing with biochemical mutational scanning experiments, finding strong quantitative agreement, even between different organisms. We also found that the correlation of mutation fitness effects was not affected by protein solvent exposure or structural disorder. Together, our results suggest that the correlation of fitness effects at the same site is a previously overlooked yet fundamental property of protein evolution.

Evolutionary Biology↗

bioRxiv2015

Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens

Despite the global economic and ecological importance of forest trees, the genomic basis of differential adaptation and speciation in tree species is still poorly understood. Populus tremula and P. tremuloides are two of the most widespread tree species in the Northern Hemisphere. Using whole-genome re-sequencing data of 24 P. tremula and 22 P. tremuloides individuals, we find that the two species diverged [~]2.2-3.1 million years ago, coinciding with the severing of the Bering land bridge and the onset of dramatic climatic oscillations during the Pleistocene. Both species have experienced substantial population expansions following long-term declines after species divergence. We detect widespread and heterogeneous genomic differentiation between species, and in accordance with the expectation of allopatric speciation, coalescent simulations suggest that neutral evolutionary processes can account for most of the observed patterns of genomic differentiation. However, there is an excess of regions exhibiting extreme differentiation relative to those expected under demographic simulations, which is indicative of the action of natural selection. Overall genetic differentiation is negatively associated with recombination rate in both species, providing strong support for a role of linked selection in generating the heterogeneous genomic landscape of differentiation between species. Finally, we identify a number of candidate regions and genes that may have been subject to positive and/or balancing selection during the speciation process.

Evolutionary Biology↗

bioRxiv2016

Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians

The diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids--distantly related animals considered to be segmented. Far less is known about the role of \"segmentation genes\" in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods--marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects--except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis.

Evolutionary Biology↗

bioRxiv2015

Adaptation to heavy-metal contaminated environments proceeds via selection on pre-existing genetic variation

Anthropogenic environmental changes create evolutionary pressures on populations to adapt to novel stresses. It is as yet unclear, when populations respond to these selective pressures, the extent to which this results in convergent genetic evolution and whether convergence is due to independent mutations or shared ancestral variation. We address these questions using a classic example of adaptation by natural selection by investigating the rapid colonization of the plant species Mimulus guttatus to copper contaminated soils. We use field-based reciprocal transplant experiments to demonstrate that mine alleles at a major copper tolerance locus, Tol1, are strongly selected in the mine environment. We assemble the genome of a mine adapted genotype and identify regions of this genome in tight genetic linkage to Tol1. We discover a set of a multicopper oxidase genes that are genetically linked to Tol1 and exhibit large differences in expression between tolerant and non-tolerant genotypes. We overexpressed this gene in M. guttatus and A. thaliana and found the introduced gene contributes to enhanced copper tolerance. We identify convergent adaptation loci that are additional to Tol1 by measuring genome-wide differences in allele frequency between pairs of mine and off-mine populations and narrow these regions to specific candidate genes using differences in protein sequence and gene expression. Furthermore, patterns of genetic variation at the two most differentiated candidate loci are consistent with selection acting upon alleles that predates the existence of the copper mine habitat. These results suggest that adaptation to the mine habitat occurred via selection on ancestral variation, rather than independent de novo mutations or migration between populations.

Evolutionary Biology↗