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bioRxiv2016

Recent advances in the study of fine-scale population structure in humans

Empowered by modern genotyping and large samples, population structure can be accurately described and quantified even when it only explains a fraction of a percent of total genetic variance. This is especially relevant and interesting for humans, where fine-scale population structure can both confound disease-mapping studies and reveal the history of migration and divergence that shaped our species diversity. Here we review notable recent advances in the detection, use, and understanding of population structure. Our work addresses multiple areas where substantial progress is being made: improved statistics and models for better capturing differentiation, admixture, and the spatial distribution of variation; computational speed-ups that allow methods to scale to modern data; and advances in haplotypic modeling that have wide ranging consequences for the analysis of population structure. We conclude by outlining four important open challenges: The limitations of discrete population models, uncertainty in individual origins, the incorporation of both fine-scale structure and ancient DNA in parametric models, and the development of efficient computational tools, particularly for haplotype-based methods.

Evolutionary Biology↗

bioRxiv2016

High throughput sequencing of multiple amplicons for barcoding and integrative taxonomy

Until now, the potential of NGS has been seldom realised for the construction of barcode reference libraries. Using a two-step PCR approach and MiSeq sequencing, we tested a cost-effective method and developed a custom workflow to simultaneously sequence multiple markers (COI, Cytb and EF, altogether 2kb) from hundreds of specimens. Interestingly, primers and PCR conditions used for Sanger sequencing did not require optimisation to construct MiSeq library. After completion of quality controls, 87% of the species and 76% of the specimens had valid sequences for the three markers. Nine specimens (3%) exhibited two divergent (up to 10%) sequence clusters. In 95% of the species, MiSeq and Sanger sequences obtained from the same samplings were similar. For the remaining 5%, species were paraphyletic or the sequences clustered into two divergent groups (>7%) on the final trees (Sanger + MiSeq). These problematic cases are difficult to explain but may represent coding NUMTS or heteroplasms. These results highlight the importance of performing quality control steps, working with expert taxonomists and using more than one marker for DNA-taxonomy or species diversity assessment. The power and simplicity of this method appears promising to build on existing experience, tools and resources while taking advantage of NGS.

Evolutionary Biology↗

bioRxiv2016

Fossils matter: improved estimates of divergence times in Pinus reveal older diversification

BackgroundThe taxonomy of the genus Pinus is widely accepted and a well-resolved phylogeny based on entire plastome sequences exists. However, there is a large discrepancy in estimated divergence times of major pine clades among existing studies mainly due to differences in fossil placement and dating methods used. We currently lack a dated molecular pine phylogeny that makes full usage of the rich fossil record in pines. This study is the first to estimate the divergence dates of pines based on a large number of fossils (21) evenly distributed across all major clades in combination with applying the most novel dating method.\n\nResultsWe present a range of molecular phylogenetic trees of Pinus generated within a Bayesian framework using both the novel fossilized birth-death and the traditional node dating method with different fossil sets. We find the origin of pines likely to be up to 30 Myr older (Early Cretaceous) than inferred in most previous studies (Late Cretaceous) and propose generally older divergence times for major clades within Pinus than previously thought. Our age estimates vary significantly between the different dating approaches but the results generally agree on older divergence times. We present a revised list of 21 fossils that are suitable to use in dating or comparative analyses of pines.\n\nConclusionsAn accurate timescale for the divergence times in pines is essential if we are to link diversification processes and functional adaptation of this genus to geological events or to changing climates. Next to older divergence times in Pinus, our results indicate that node age estimates in pines depend on dating approaches and fossil sets used due to different inherent characteristics of dating approaches. Our set of dated phylogenetic trees of pines presented herein provide the basis to account for uncertainties in age estimations when applying comparative phylogenetic methods, which will improve our understanding of the evolutionary and ecological history in pines.

Evolutionary Biology↗

bioRxiv2016

Range stability predicts lineage persistence in a morphologically cryptic ground squirrel species complex

The processes responsible for patterns of cytonuclear discordance remain unclear. Here, we employ an exon capture dataset, demographic methods, and species distribution modeling to elucidate the impact of historical demography on patterns of genealogical concordance and discordance in ground squirrel lineages from the Otospermophilus beecheyi species complex. Previous studies in O. beecheyi revealed three morphologically cryptic and highly divergent mitochondrial DNA (mtDNA) lineages (named the Northern, Central, and Southern lineages based on geography) with only the Northern lineage exhibiting concordant divergence in nuclear markers. We show that these mtDNA lineages likely formed in allopatry during the Pleistocene, but responded differentially to climatic changes that occurred since the last interglacial ([~]120,000 years ago). We find that the Northern lineage maintained a stable range throughout this period, correlating with genetic distinctiveness among all genetic markers and low migration rates between the other lineages. In contrast, our results support a scenario where the Southern lineage expanded from Baja California Sur during the Late Pleistocene and hybridized with the Central lineage, eventually driving the Central lineage to extinction. While high intraspecific gene flow among newly colonized populations eroded significant signals of Central ancestry from autosomal markers, male sex-biased dispersal in this system preserved signals of this past hybridization and introgression event in matrilineal-biased X-chromosome and mtDNA markers. Our results highlight the importance of range stability in maintaining the persistence of phylogeographic lineages, whereas unstable range dynamics can increase the tendency for lineages to interact and collapse upon secondary contact.

Evolutionary Biology↗

bioRxiv2016

Comparative genomics and metagenomics analyses of endangered Père David’s deer (Elaphurus davidianus) provide insights into population recovery

The milu (Pere Davids deer, Elaphurus davidianus) has become a classic example of how highly endangered animal species can be rescued. However, the mechanisms that underpinned this population recovery remain largely unknown. As part of this study, we sequenced and analyzed whole genomes from multiple captive individuals. Following this analysis, we observed that the milu experienced a prolonged population decline over the last 200,000 years, which led to an elongated history of inbreeding. This protracted inbreeding history facilitated the purging of deleterious recessive alleles, thereby ameliorating associated threats to population viability. Because of this phenomenon, milu are now believed to be less susceptible to future inbreeding depression occurrences. SNP distribution patterns confirmed inbreeding history and also indicated sign of increased and increasing diversity in the recovered milu population. A selective sweep analysis identified two outlier genes (CTSR2 and GSG1) that were related to male fertility. Furthermore, we observed strong signatures of selection pertaining to the host immune system, including six genes (SERPINE1, PDIA3, CD302, IGLL1, VPREB3, and CD53 antigen), which are likely to strengthen resistance to pathogens. We also identified several adaptive features including the over-representation of gene families encoding for olfactory receptor activity, a high selection pressure pertaining to DNA repair and host immunity, and tolerance to high-salt swamp diets. Moreover, glycan biosynthesis, lipid metabolism, and cofactor and vitamin metabolism were all significantly enriched in the gut microbiomes of milu. We speculate that these characteristics play an important role in milu energy metabolism, immunity, development, and health. In conclusion, our findings provide a unique insight into animal population recovery strategies.

Evolutionary Biology↗

bioRxiv2016

The impact of recent population history on the deleterious mutation load in humans and close evolutionary relatives

Over the past decade, there has been both great interest and confusion about whether recent demographic events--notably the Out-of-Africa-bottleneck and recent population growth--have led to differences in mutation load among human populations. The confusion can be traced to the use of different summary statistics to measure load, which lead to apparently conflicting results. We argue, however, that when statistics more directly related to load are used, the results of different studies and data sets consistently reveal little or no difference in the load of non-synonymous mutations among human populations. Theory helps to understand why no such differences are seen, as well as to predict in what settings they are to be expected. In particular, as predicted by modeling, there is evidence for changes in the load of recessive loss of function mutations in founder and inbred human populations. Also as predicted, eastern subspecies of gorilla, Neanderthals and Denisovans, who are thought to have undergone reductions in population sizes that exceed the human Out-of-Africa bottleneck in duration and severity, show evidence for increased load of non-synonymous mutations (relative to western subspecies of gorillas and modern humans, respectively). A coherent picture is thus starting to emerge about the effects of demographic history on the mutation load in populations of humans and close evolutionary relatives.

Evolutionary Biology↗

bioRxiv2016

Molecular adaptation in Rubisco: discriminating between convergent evolution and positive selection using mechanistic and classical codon models

Rubisco (Ribulose-1, 5-biphosphate carboxylase/oxygenase) is the most important enzyme on earth, catalyzing the first step of CO2 fixation in photosynthesis. Its molecular adaptation to C4 photosynthetic pathway has attracted a lot of attention. C4 plants, which comprise less than 5% of land plants, have evolved more efficient photosynthesis compared to C3 plants. Interestingly, a large number of independent transitions from C3 to C4 phenotype have occurred. Each time, the Rubisco enzyme has been subject to similar changes in selective pressure, thus providing an excellent model for convergent evolution at the molecular level. Molecular adaptation is often identified with positive selection and is typically characterized by an elevated ratio of non-synonymous over synonymous substitution rates (dN/dS). However, convergent adaptation is expected to leave a different molecular signature, taking the form of repeated transitions toward identical or similar amino acids.\n\nHere, we use a previously introduced codon-based differential selection model to detect and quantify consistent patterns of convergent adaptation in Rubisco in Amaranthaceae. We further contrast the results thus obtained with those obtained under classical codon models based on the estimation of dN/dS. We find that the two classes of models tend to select distinct, although overlapping, sets of positions. This discrepancy in the results illustrates the conceptual difference between these models, while emphasizing the need to better discriminate between qualitatively different selective regimes, by using a broader class of codon models than those currently considered in molecular evolutionary studies.

Evolutionary Biology↗

bioRxiv2016

The Impact of Migratory Flyways on the Spread of Avian Influenza Virus in North America

Wild birds are the major reservoir hosts for influenza A viruses (AIVs) and have been implicated in the emergence of pandemic events in livestock and human populations. Understanding how AIVs spread within and across continents is therefore critical to the development of successful strategies to manage and reduce the impact of influenza outbreaks. In North America many bird species undergo seasonal migratory movements along a North-South axis, thereby fostering opportunities for viruses to spread over long distances. However, the role played by such avian flyways in shaping the genetic structure of AIV populations has proven controversial. To assess the relative contribution of bird migration along flyways to the genetic structure of AIV we performed a large-scale phylogeographic study of viruses sampled in the USA and Canada, involving the analysis of 3805 to 4505 sequences from 36 to 38 geographic localities depending on the gene data set. To assist this we developed a maximum likelihood-based genetic algorithm to explore a wide range of complex spatial models, thereby depicting a more complete picture of the migration network than previous studies. Based on phylogenies estimated from nucleotide data sets, our results show that AIV migration rates within flyways are significantly higher than those between flyways, indicating that the migratory patterns of birds play a key role in pathogen dispersal. These findings provide valuable insights into the evolution, maintenance and transmission of AIVs, in turn allowing the development of improved programs for surveillance and risk assessment.\n\nSignificance StatementAvian influenza viruses infect a wide variety of wild bird species and represent a potential disease threat to the poultry industry and hence to human and livestock populations. However, the ecological factors that drive the geographic spread and evolution of these viruses are both poorly understood and controversial at the continental scale, particularly the role played by migratory flyways in shaping patterns of virus dispersal. Using a novel phylogeographic analysis of large genomic data sets we show migration flyways act as important transmission barriers to the spread of avian influenza viruses in North America. Hence, these results indicate that the spread of avian influenza virus in wild birds in North America has an element of predictability.

Evolutionary Biology↗

bioRxiv2016

The species problem from the modeler’s point of view

How to define a partition of individuals into species is a long-standing question called the species problem in systematics. Here, we focus on this problem in the thought experiment where individuals reproduce clonally and both the differentiation process and the population genealogies are explicitly known. We point out three desirable properties of species partitions: (A) Heterotypy between species, (B) Homotypy within species and (M) Monophyly of each species. We then ask: How and when is it possible to delineate species in a way satisfying these properties?\n\nWe point out that the three desirable properties cannot in general be satisfied simultaneously, but that any two of them can. We mathematically prove the existence of the finest partition satisfying (A) and (M) and the coarsest partition satisfying (B) and (M). For each of them, we propose a simple algorithm to build the associated phylogeny out of the genealogy.\n\nThe ways we propose to phrase the species problem shed new light on the interaction between the genealogical and phylogenetic scales in modeling work. The two definitions centered on the monophyly property can readily be used at a higher taxonomic level as well, e.g. to cluster species into monophyletic genera.

Evolutionary Biology↗

bioRxiv2016

Multiple factors influence population sex ratios in the Mojave Desert moss Syntrichia caninervis

O_LIPremise of research: Natural populations of many mosses appear highly female-biased based on the presence of reproductive structures. This bias could be caused by increased male mortality, lower male growth rate, or a higher threshold for achieving sexual maturity in males. Here we test these hypotheses using samples from two populations of the Mojave Desert moss Syntrichia caninervis.\nC_LIO_LIMethods: We used double digest restriction-site associated DNA (RAD) sequencing to identify candidate sex-associated loci in a panel of sex-expressing plants. Next, we used putative sex-associated markers to identify the sex of individuals without sex structures.\nC_LIO_LIKey results: We found an 18:1 phenotypic female: male sex ratio in the higher elevation site (Wrightwood), and no sex expression at the low elevation site (Phelan). In contrast, based on genetic data we found a 2:1 female bias in the Wrightwood site and only females in the Phelan site. The area occupied by male and female genets was indistinguishable.\nC_LIO_LIConclusions: These data suggest that both differential mortality and sexual dimorphism in thresholds for sex expression likely contribute to population genetic and phenotypic sex ratio biases, and that phenotypic sex expression alone fails to capture the extent of actual sex ratio bias present in natural populations of S. caninervis.\nC_LI

Evolutionary Biology↗

bioRxiv2016

Pre-metazoan origin of animal miRNAs

microRNAs (miRNAs) are integrated parts of the developmental toolkit in animals. The evolutionary history and origins of animal miRNAs is however unclear, and it is not known when they evolved and on how many occasions. We have therefore investigated the presence of miRNAs and the necessary miRNA biogenesis machinery in a large group of unicellular relatives of animals, Ichthyosporea. By small RNA sequencing we find evidence for at least four genes in the genus Sphaeroforma that satisfy the criteria for the annotation of animal miRNA genes. Three of these miRNAs are conserved and expressed across sphaeroformid species. Furthermore, we identify homologues of the animal miRNA biogenesis genes across a wide range of ichthyosporeans, including Drosha and Pasha which make up the animal specific Microprocessor complex. Taken together we report the first evidence for bona fide miRNA genes and the presence of the miRNA-processing pathway in unicellular Choanozoa, implying that the origin of animal miRNAs and the Microprocessor complex predates multicellular animals.

Evolutionary Biology↗

bioRxiv2016

The Melting Snowball: A Test of the Snowball Model Using RNA

Genetic incompatibilities can emerge as a by-product of genetic divergence. According to Dobzhansky and Muller, alleles at different loci that have fixed in different genetic backgrounds may be incompatible when brought together in a hybrid. Orr showed that the number of Dobzhansky-Muller incompatibilities (DMIs) should accumulate faster than linearly--i.e., snowball--as two lineages diverge. Several studies have attempted to test the snowball model using data from natural populations. One limitation of these studies is that they have focused on predictions of the snowball model but not on its underlying assumptions. Here we use a computational model of RNA folding to test both predictions and assumptions of the snowball model. In this model, two populations are allowed to evolve in allopatry on a holey fitness landscape. We find that the number of DMIs involving pairs of loci (i.e., simple DMIs) does not snowball--rather, it increases approximately linearly with divergence. We show that the probability of emergence of a simple DMI is approximately constant, as assumed by the snowball model. However, simple DMIs can disappear after they have arisen, contrary to the assumptions of the snowball model. This occurs because simple DMIs become complex (i.e., involve alleles at three or more loci) as a result of later substitutions. We introduce a modified snowball model--the melting snowball model--where simple DMIs can become complex after they appear. The melting snowball model can account for the results of the RNA folding model. We also find that complex DMIs are common and, unlike simple ones, do snowball. Reproductive isolation, however, does not snowball because DMIs do not act independently of each other. We conclude that the RNA folding model supports the central prediction of the snowball model that the number of DMIs snowballs, but challenges some of its underlying assumptions.

Evolutionary Biology↗

bioRxiv2016

Deep-time parallel evolution of myrmecoid syndrome in rove beetle symbionts of army ants

Recent adaptive radiations provide striking examples of convergence, but the predictability of evolution over much deeper timescales is controversial, due to a scarcity of ancient clades exhibiting repetitive patterns of phenotypic evolution. Army ants are ecologically dominant arthropod predators of the world's tropics, with large nomadic colonies housing diverse communities of socially parasitic myrmecophiles. Remarkable among these are many species of rove beetle (Staphylinidae) that exhibit ant-mimicking \"myrmecoid\" body forms and are behaviorally accepted into their aggressive hosts' societies: emigrating with colonies and inhabiting temporary nest bivouacs, grooming and feeding with workers, but also consuming the brood. Here we demonstrate that myrmecoid rove beetles are strongly polyphyletic, with this novel adaptive morphological and behavioral syndrome having evolved at least twelve times during the evolution of a single staphylinid subfamily, Aleocharinae. Each independent myrmecoid clade is restricted to one zoogeographic region and highly host-specific on a single army ant genus. Dating estimates reveal that myrmecoid clades are separated by substantial phylogenetic distances--as much as 105 million years (My). All such groups arose in parallel during the Cenozoic, as army ants are proposed to have risen to ecological dominance. This work uncovers a rare example of an ancient system of complex morphological and behavioral convergence, with replicate beetle lineages following a predictable phenotypic trajectory during their parasitic coevolution with army ants.

Evolutionary Biology↗

bioRxiv2016

Seasonal influenza circulation patterns and projections for 2016-2017

This is not meant as a comprehensive report, but is instead intended as particular observations that may be of relevance. Please also note that observed patterns reflect the GISAID database and may not be entirely representative of underlying dynamics. All analyses are based on the nextflu pipeline [1] with continual updates posted to Correspondence:http://nextflu.org.

Evolutionary Biology↗

bioRxiv2016

Larger Numbers can Impede Adaptation in Microbial Populations despite Entailing Greater Genetic Variation

Periodic bottlenecks play a major role in shaping the adaptive dynamics of natural and laboratory populations of asexual microbes. Here we study how they affect the Extent of Adaptation (EoA), in such populations. EoA, the average fitness gain relative to the ancestor, is the quantity of interest in a large number of microbial experimental-evolution studies which assume that for any given bottleneck size (N0) and number of generations between bottlenecks (g), the harmonic mean size (HM=N0g) will predict the ensuing evolutionary dynamics. However, there are no theoretical or empirical validations for HM being a good predictor of EoA. Using experimental-evolution with Escherichia coli and individual-based simulations, we show that HM fails to predict EoA (i.e., higher N0g does not lead to higher EoA). This is because although higher g allows populations to arrive at superior benefits by entailing increased variation, it also reduces the efficacy of selection, which lowers EoA. We show that EoA can be maximized in evolution experiments by either maximizing N0 and/or minimizing g. We also conjecture that N0/g is a better predictor of EoA than N0g. Our results call for a re-evaluation of the role of population size in predicting fitness trajectories. They also aid in predicting adaptation in asexual populations, which has important evolutionary, epidemiological and economic implications.

Evolutionary Biology↗

bioRxiv2016

EARLY INFLAMMATION, IMMUNOPATHOLOGY AND AGING

Age-related diseases are often attributed to immunopathology, which results in self-damage caused by an inappropriate inflammatory response. Immunopathology associated with early-life inflammation also appears to cause faster ageing, although we lack direct experimental evidence for this association. To understand the interactions between ageing, inflammation and immunopathology, we used the mealworm beetle Tenebrio molitor as a study organism. We hypothesized that phenoloxidase (PO), an important immune effector in insect defence, may impose substantial immunopathological costs by causing tissue damage, in turn accelerating aging. In support of this hypothesis, we found that RNAi knockdown of PO transcripts in young adults reduced inflammation-induced autoreactive tissue damage to Malpighian tubules, and increased adult lifespan. Our work thus provides empirical evidence for a causative link between immunopathological costs of early life inflammation and faster ageing. We also reasoned that if natural selection weakens with age, older individuals should display increased immunopathological costs associated with an immune response. Indeed, we found that while old infected individuals cleared infection faster than young individuals, they displayed exacerbated immunopathological costs and higher post-infection mortality. RNAi-mediated knockdown of PO response reduced immunopathology in older beetles and increased their lifespan after infection. This is the first demonstration of a direct role of immunopathological consequences of immune response during ageing in insects. Our work is also the first report that highlights the pervasive role of immunopathology under diverse contexts of aging and immune response.

Evolutionary Biology↗

bioRxiv2016

The Opiliones Tree of Life: shedding light on harvestmen relationships through transcriptomics

Opiliones are iconic arachnids with a Paleozoic origin and a diversity that reflects ancient biogeographical patterns dating back at least to the times of Pangea. Due to interest in harvestman diversity, evolution and biogeography, their relationships have been thoroughly studied using morphology and PCR-based Sanger approaches to systematics. More recently, two studies utilized transcriptomics-based phylogenomics to explore their basal relationships and diversification, but sampling was limiting for understanding deep evolutionary patterns, as they lacked good taxon representation at the family level. Here we analyze a set of the 14 existing transcriptomes with 40 additional ones generated for this study, representing ca. 80% of the extant familial diversity in Opiliones. Our phylogenetic analyses, including a set of data matrices with different gene occupancy and evolutionary rates, and using a multitude of methods correcting for a diversity of factors affecting phylogenomic data matrices, provide a robust and stable Opiliones tree of life, where most families are precisely placed. Our dating analyses also using alternative calibration points, methods, and analytical parameters provide well-resolved old divergences, consistent with ancient regionalization in Pangea in some groups, and Pangean vicariance in others. The integration of state-of-the-art molecular techniques and analyses, together with the broadest taxonomic sampling to date presented in a phylogenomic study of harvestmen, provide new insights into harvestmen interrelationships, as well as a general overview of the general biogeographic patterns of this ancient arthropod group.

Evolutionary Biology↗

bioRxiv2016

The genetic basis and fitness consequences of sperm midpiece size in deer mice

An extraordinary array of reproductive traits vary among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive. Here we examine two sister-species of Peromyscus mice with divergent mating systems. We find that the promiscuous species produces sperm with longer midpiece than the monogamous species, and midpiece size correlates positively with competitive ability and swimming performance. Using forward genetics, we identify a gene associated with midpiece length: Prkar1a, which encodes the R1 regulatory subunit of PKA. R1 localizes to midpiece in Peromyscus and is differentially expressed in mature sperm of the two species yet is similarly abundant in the testis. We also show that genetic variation at this locus accurately predicts male reproductive success. Our findings suggest that rapid evolution of reproductive traits can occur through cell type-specific changes to ubiquitously expressed genes and have an important effect on fitness.

Evolutionary Biology↗