Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origin of ecotypes is often inferred on the basis of a phylogeny which clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic due to the potential for gene flow and incomplete lineage sorting to uncouple the...
Adaptation to novel environments often involves the evolution of multiple morphological, physiological and behavioral traits. One striking example of multi-trait evolution is the suite of traits that has evolved repeatedly in cave animals, including regression of eyes, loss of pigmentation, and enhancement of non-visual sensory systems. The Mexican tetra, Astyanax mexicanus, consists of fish that inhabit at least 30 caves in Northeast Mexico and ancestral-like surface fish which inhabit the rivers...
Emerging evidence has demonstrated that urbanization shapes the ecology and evolution of species interactions. Islands are particularly susceptible to urbanization due to the fragility of their ecosystems; however, few studies have examined the effects of urbanization on species interactions on islands. To address this gap, we studied the effects of urbanization on interactions between Darwin's finches and its food source, Tribulus cistoides, on three towns in the Galapagos Islands. We assessed the...
Phylogenetic divergence-time estimation has been revolutionized by two recent developments: 1) total-evidence dating (or "tip-dating") approaches that allow for the incorporation of fossils as tips in the analysis, with their phylogenetic and temporal relationships to the extant taxa inferred from the data, and 2) the fossilized birth-death (FBD) class of tree models that capture the processes that produce the tree (speciation, extinction, and fossilization), and thus provide a coherent and biologically...
Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide spray to the expression changes that evolve in response...
A major question in evolution is how to maintain many adaptive phenotypes within a species. In Mediterranean wild thyme, a staggering number of discrete chemical phenotypes (chemotypes) coexist in close geographic proximity. Plant chemotypes are defined by the dominant monoterpene produced in their essential oil. We study the genetics of six distinct chemotypes nested within two well established ecotypes. Ecotypes, and chemotypes within ecotypes, are spatially segregated, and their distribution tracks...
The phage shock protein (Psp) stress-response system protects bacteria from envelope stress and stabilizes the cell membrane. Recent work from our group suggests that the psp systems have evolved independently in distinct Gram-positive and Gram-negative bacterial clades to effect similar stress response functions. Despite the prevalence of the key effector, PspA, and the functional Psp system, the various genomic contexts of Psp proteins, as well as their evolution across the kingdoms of life, have...
Most phenotypes, such as gene expression profiles, developmental trajectories, behavioural sequences or other reaction norms are function-valued traits, since they vary across an individuals age and in response to various internal and/or external factors (state variables). In turn, many individuals live in populations subject to some limited genetic mixing and are thus likely to interact with their relatives. We here formalise selection on function-valued traits when individuals interact in a group-structured...
The introduction of non-native species into new habitats is one of the foremost risks to global biodiversity. Here, we evaluate a recent invasion of wild tomato (Solanum pimpinellifolium) onto the Galapagos islands from a population genomic perspective, using a large panel of novel collections from the archipelago as well as historical accessions from mainland Ecuador and Peru. We infer a recent invasion of S. pimpinellifolium on the islands, largely the result of a single event from central Ecuador...
How the avian sex chromosomes first evolved from autosomes remains elusive as 100 million years (Myr) of divergence and degeneration obscure their evolutionary history. Sylvioidea songbirds is an emerging model for understanding avian sex chromosome evolution because a unique chromosome fusion event ~24 Myr ago has formed enlarged "neo-sex chromosomes" consisting of an added (new) and an ancestral (old) part. Here, we report the female genome (ZW) of one Sylvioidea species, the great reed warbler...
Although observed in many interspecific crosses, the genetic basis of most hybrid incompatibilities is still unknown. Mismatches between parental genomes in selfish elements and the genes that regulate these elements are frequently hypothesized to underlie hybrid dysfunction. We evaluated the potential role of transposable elements (TEs) in hybrid incompatibilities by examining hybrids between Drosophila virilis strains polymorphic for TEs that cause dysgenesis and a closely related species that...
Nitrogen is an essential element to life and exerts a strong control on global biological productivity. The rise and spread of nitrogen-utilizing microbial metabolisms profoundly shaped the biosphere on the early Earth. Here we reconciled gene and species trees to identify birth and horizontal gene transfer events for key nitrogen-cycling genes, dated with a time-calibrated tree of life, in order to examine the timing of the proliferation of these metabolisms across the tree of life. Our results...
Mitochondria retain their own genomes as other bacterial endosymbiont-derived organelles. Nevertheless, no protein for DNA replication and repair is encoded in any mitochondrial genomes (mtDNAs) assessed to date, suggesting the nucleus primarily governs the maintenance of mtDNA. As the proteins of diverse evolutionary origins occupy a large proportion of the current mitochondrial proteomes, we anticipate finding the same evolutionary trend in the nucleus-encoded machinery for mtDNA maintenance. Indeed,...
BackgroundExperimental evolution of microbes can be used to empirically address a wide range of questions about evolution and is increasingly employed to study complex phenomena ranging from genetic evolution to evolutionary rescue. Regardless of experimental aims, fitness assays are a central component of this type of research, and low-throughput often limits the scope and complexity of experimental evolution studies. We created an experimental evolution system in Saccharomyces cerevisiae that utilizes...
Recent results comparing the temporal program of genome replication of yeast species belonging to the Lachancea clade support the scenario that the evolution of replication timing program could be mainly driven by correlated acquisition and loss events of active replication origins. Using these results as a benchmark, we develop an evolutionary model defined as birth-death process for replication origins, and use it to identify the selective pressures that shape the replication timing profiles. Comparing...
AbstractHybridization and genome duplication have played crucial roles in the evolution of many animal and plant taxa. During their evolution, the subgenomes of parental species undergo considerable changes in hybrids and polyploids, which often selectively eliminate segments of one subgenome. However, the mechanisms underlying these changes are not well understood, particularly when the hybridization is linked with asexual reproduction that may enforce specific evolutionary pathways. We studied...
Sexual selection researchers have traditionally focused on adult sex differences; however, the schedule and pattern of sex-specific ontogeny can provide insights unobtainable from an exclusive focus on adults. Recently, it has been debated whether facial width-to-height ratio (fWHR; bi-zygomatic breadth divided by midface height) is a human secondary sexual characteristic (SSC). Here, we review current evidence, then address this debate using ontogenetic evidence, which has been under-explored in...
Approximately 100 years ago, hunter-harvest eliminated white-tailed deer (WTD; Odocoileus virginianus) in eastern North America, which subsequently served as a catalyst for wildlife management as a national priority. An extensive stock-replenishment effort soon followed, with WTD broadly translocated among states as a means of reestablishment. Now, contemporary issues focus on reverberations from a global (and fatal) epizootic disease in Cervidae (chronic wasting disease, CWD). These cumulative impacts...
A long standing hypothesis is that divergence between humans and chimpanzees might have been driven more by regulatory level adaptions than by protein sequence adaptations. This has especially been suggested for regulatory adaptions in the evolution of the human brain. There is some support for this hypothesis, but it has been limited by the lack of a reliable and powerful way to detect positive selection on regulatory sequences. We present a new method to detect positive selection on transcription...
Background: The nucleotide composition of the genome is a balance between origin and fixation rates of different mutations. For example, it is well-known that transitions occur more frequently than transversions, particularly at CpG sites. Differences in fixation rates of mutation types are less explored. Specifically, recombination-associated GC-biased gene conversion (gBGC) may differentially impact GC-changing mutations, due to differences in their genomic distributions and efficiency of mismatch...
Although combination antiretoviral therapies seem to be effective at controlling HIV-1 infections regardless of the viral subtype, there is increasing evidence for subtype-specific drug resistance mutations. The order and rates at which resistance mutations accumulate in different subtypes also remain poorly understood. Here, we present a methodology for the comparison of mutational pathways in different HIV-1 subtypes, based on Hidden Conjunctive Bayesian Networks (H-CBN), a probabilistic model...
Inbreeding depression is a central parameter underlying mating system variation in nature and one that can be altered by environmental stress. Although a variety of systems show that inbreeding depression tends to increase under stressful conditions, we have very little understanding across most organisms how the level of inbreeding depression may change as a result of adaptation to stressors. In this work we examined the potential that inbreeding depression varied among lineages of Ipomoea purpurea...
Despite the importance of gene function to evolutionary biology, the applicability of comparative methods to gene function is poorly known. A specific case which has crystalized methodological questions is the "ortholog conjecture", the hypothesis that function evolves faster after duplication (i.e., in paralogs), and conversely conserved between orthologs. Since the mode of functional evolution after duplication is not well known, we investigate under what reasonable evolutionary scenarios phylogenetic...
The evolution of vertebrates from an invertebrate chordate ancestor involved the evolution of new organs, tissues, and cell types. It was also marked by the origin and duplication of new gene families. If, and how, these morphological and genetic innovations are related is an unresolved question in vertebrate evolution. Hyaluronan is an extracellular matrix (ECM) polysaccharide important for water homeostasis and tissue structure. Vertebrates possess a novel family of hyaluronan binding proteins...
Gene and genome duplications are essential processes in evolution. Salmonids are ideal animal model systems to study these processes, as they originated from a tetraploid ancestor. Conserved non-coding elements (CNEs) are of interest because of their highly conserved DNA consensus motifs spanning lineages as diverse and divergent as humans and fish. The main goal of this study is to test CNEs as a tool to study genome duplications and to revisit the "4R" hypothesis and phylogeny of Salmonine fishes...
How microbes affect host fitness and environmental adaptation has become a fundamental research question in evolutionary biology. We tested for associations of bacterial genomic variation and Drosophila melanogaster offspring number in a microbial Genome Wide Association Study (GWAS). Leveraging strain variation in the genus Gluconobacter, a genus of bacteria that are commonly associated with Drosophila under natural conditions, we pinpoint the thiamine biosynthesis pathway (TBP) as contributing...
The maternal inheritance of mitochondrial genomes entails a sex-specific selective sieve, whereby mutations in mitochondrial DNA can only respond to selection acting directly on females. In theory, this enables male-harming mutations to accumulate in mitochondrial genomes if they are neutral, beneficial, or only slightly deleterious to females. Ultimately, this bias could drive the evolution of male-specific mitochondrial mutation loads, an idea known as mothers curse. Earlier work on this hypothesis...
By altering gene expression and creating paralogs, genomic amplifications represent a key component of short-term adaptive processes. In insects, the use of insecticides can select gene amplifications causing an increased expression of detoxification enzymes, supporting their usefulness for monitoring the dynamics of resistance alleles in the field. In this context, the present study aims to characterise a genomic amplification event associated with resistance to organophosphate insecticides in the...
LTR-retrotransposons are structurally similar to retroviruses, as they possess the enzymes reverse transcriptase, Ribonuclease H, integrase, proteinase, and the gag gene and are flanked by long terminal repeats (LTRs). The 412/mdg1 lineage, belonging to the Ty3/Gypsy group, consists of the TEs 412, mdg1, stalker, pilgrim, and blood. The 412/mdg1 lineage is distinguished from the others in the gypsy group in that it has small ORFs at the beginning of the TE and is highly similar to the pol ORF among...
Distribution history of the widespread Neotropical genus Hypostomus to shed light on the processes that shaped species diversity. We inferred a calibrated phylogeny; ancestral habitat preference, ancestral areas distribution, and the history of dispersal and vicariance events of this genus. The phylogenetic and distributional analyses indicate that Hypostomus species inhabiting La Plata Basin do not form a monophyletic clade, suggesting that several unrelated ancestral species colonized this basin...
Severe acute respiratory syndrome coronavirus 2, SARS-CoV-2, was quickly identified as the cause of COVID-19 disease soon after its earliest reports. The knowledge of the contemporary evolution of SARS-CoV-2 is urgently needed not only for a retrospective on how, when, and why COVID-19 has emerged and spread, but also for creating remedies through efforts of science, technology, medicine, and public policy. Global sequencing of thousands of genomes has revealed many common genetic variants, which...
Some stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we produce a chromosome-level genome assembly of the stalk-eyed fly, T. dalmanni, to elucidate the pattern of genomic divergence associated with the presence of drive elements. We find evidence for multiple nested inversions along the sex ratio haplotype and widespread differentiation and divergence between the inversion types...
The Hypostomini tribe comprises a single genus, Hypostomus, which possibly contains several monophyletic groups because of significant morphological variation and a variety of diploid numbers and karyotype formulas. The objective of this study was to infer evolutionary relationships among some species of Hypostomus found in the Parana River basin and subsequently to identify chromosomal synapomorphies in the groupings formed. Two nuclear genes, rag1 and rag2, and two mitochondrial genes, mt-co1 and...
BackgroundCladobranch sea slugs represent roughly half of the biodiversity of soft-bodied, marine gastropod molluscs (Nudibranchia) on the planet. Despite their global distribution from shallow waters to the deep sea, from tropical into polar seas, and their important role in marine ecosystems and for humans (as bioindicators and providers of medical drug leads), the evolutionary history of cladobranch sea slugs is not yet fully understood. Here, we amplify the current knowledge on the phylogenetic...
We present a concept that summarizes the pattern of occurrence of widely distributed organisms with large chromosomal diversity, low molecular divergence, and the absence of morphological identity. Our model is based on cytogenetic and molecular data of four populations of the siluriform Hypostomus ancistroides presented in this study in comparison with those of 15 other previously described populations but is applicable to any group of sister species, chronospecies, or cryptic species. Through the...
Motivated by recent experiments on an antibiotic resistance gene, we investigate genetic interactions between synonymous mutations in the framework of exclusion models of translation. We show that the range of possible interactions is markedly different depending on whether translation efficiency is assumed to be proportional to ribosome current or ribosome speed. In the first case every mutational effect has a definite sign that is independent of genetic background, whereas in the second case the...
The fate of duplicated genes includes pseudo-, sub-, or neo-functionalization. When different copies of a duplicated gene are pseudo-functionalized in different genotypes, genetic incompatibilities can arise in their hybrid offspring. While such cases have been reported after manual crosses, it remains unclear whether they occur in nature and how they affect natural populations. Using the Arabidopsis multi-parental RIL population, we identified four duplicated-gene based incompatibilities including...
DNA methylation-based biomarkers of aging (epigenetic clocks) promise to lead to new insights in the evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic aging effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual roe deer (Capreolus capreolus) living in two wild populations (Chize and Trois Fontaines, France) facing different ecological contexts to investigate...
Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species -the framework-builders of coral reefs- remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by uncovering a wealth of "cryptic diversity", but the ecological relevance of this diversity remains largely unclear. Here, we present an annotated draft genome for one of the most ubiquitous coral species in the Indo-Pacific (Pachyseris speciosa), and establish...
Insects use sex pheromones as a reproductive isolating mechanism to attract conspecifics and repel heterospecifics. Despite the profound knowledge of sex pheromones, little is known about the coevolutionary mechanisms and constraints on their production and detection. Using whole-genome sequences to infer the kinship among 99 drosophilids, we investigate how phylogenetic and chemical traits have interacted at a wide evolutionary timescale. Through a series of chemical syntheses and electrophysiological...
GxGxE interactions and adaptive potential of the microbiome in Drosophila melanogaster [NEW RESULTS]
The microbiome may serve as a reservoir of adaptive potential if hosts can leverage microbial adaptations in stressful environments. However, the facilitation of rapid host adaptation may be limited by interactions between host genotype, microbiome, and environment (GH x GM x E). Here, to understand how host x microbiome x environment interactions shape adaptation, we leverage >150 generations of experimental evolution in Drosophila melanogaster in a stressful environment, high sugar (HS) diet....
Infiltration of the endothelial layer of the blood-brain barrier by leukocytes plays a critical role in health and disease. When passing through the endothelial layer during the diapedesis process lymphocytes can either follow a para-cellular route or a transcellular one. There is a debate whether these two processes constitute one mechanism, or they form two evolutionary distinct migration pathways. We used phylogenetic analysis, HH search, ancestor sequence reconstruction together with functional...
Europe is the historical cradle of viticulture, but grapevines have been increasingly threatened by pathogens of American origin. The invasive oomycete Plasmopara viticola causes downy mildew, one of the most devastating grapevine diseases worldwide. Despite major economic consequences, its invasion history remains poorly understood. Comprehensive population genetic analyses of ~2000 samples from the most important wine-producing countries revealed very low genetic diversity in invasive downy mildew...
Independent origins of sociality in bees and ants are associated with independent expansions of particular odorant receptor (OR) gene subfamilies. In ants, one clade within the OR gene family, the 9-exon subfamily, has dramatically expanded. These receptors detect cuticular hydrocarbons (CHCs), key social signaling molecules in insects. It is unclear to what extent 9-exon OR subfamily expansion is associated with the independent evolution of sociality across Hymenoptera, warranting studies of taxa...
BackgroundThe emergence of a novel coronavirus (SARS-CoV-2) associated with severe acute respiratory disease (COVID-19) has prompted efforts to understand the genetic basis for its unique characteristics and its jump from non-primate hosts to humans. Tests for positive selection can identify apparently nonrandom patterns of mutation accumulation within genomes, highlighting regions where molecular function may have changed during the origin of a species. Several recent studies of the SARS-CoV-2 genome...
The 70-kDa heat shock protein (HSP70) family contains several isoforms localized in different subcellular compartments. The cytosolic isoforms have been classified into stress-inducible HSP70s and constitutive heat shock cognates (HSC70s), but occasional reports of "constitutive HSP70s" and the lack of cross-phylum comparisons have been a source of confusion in the evolution of the metazoan HSP70 family. Here we provide novel insights into the evolutionary history of this important molecular chaperone....
Closely related species that have previously inhabited geographically separated ranges are hybridizing at an increasing rate due to human disruptions. These anthropogenic hybrid zones can be used to study reproductive isolation between species at secondary contact, including examining locus-specific rates of introgression. Introgression is expected to be heterogenous across the genome, reflecting variation in selection. Those loci that introgress especially slowly are good candidates for being involved...
Exchanging genetic material with another individual seems risky from an evolutionary stand-point, and yet living things across all scales and phyla do so quite regularly. The pervasiveness of such genetic exchange, or recombination, in nature has defied explanation since the time of Darwin1-4. Conditions that favor recombination, however, are well-understood: recombination is advantageous when the genomes of individuals in a population contain more selectively mismatched combinations of alleles than...
The predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the "Red Queen hypothesis" emphasizes the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. While empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions....
Are daughters of older mothers less fertile? The human mutation rate is high and increases with chronological age. As female oocytes age, they become less functional, reducing female chances at successful reproduction. Increased oocyte mutation loads at advanced age may be passed on to offspring, decreasing fertility among daughters born to older mothers. In this paper we study the effects of maternal ageing on her daughters fertility, including total number of children, age at last birth, and neonatal...
Dietary patterns have long been a driver of global land use. Increasingly, they also respond to it, in part because of social forces that support adoption of sustainable diets. Here we develop a coupled social-land use dynamics model parameterised for 164 countries. We project global land use under 20 scenarios for future population, income, and agricultural yield. When future yields are low and/or population size is high, coupled social-land feedbacks can reduce the peak global land use by up to...
Fluctuating environmental pressures can challenge organisms by repeatedly shifting the optimum phenotype. Two contrasting evolutionary strategies to cope with these fluctuations are 1) evolution of the mean phenotype to follow the optimum (adaptive tracking) or 2) diversifying phenotypes so that at least some individuals have high fitness in the current fluctuation (bet-hedging). Bet-hedging could underlie stable differences in the behavior of individuals that are present even when genotype and environment...
Heteroplasmy is the coexistence of more than one type of mitochondria in an organism. Although widespread sequencing has identified several cases of transient or low-level heteroplasmy that primarily occur through mutation or paternal leakage, stable, high-titer heteroplasmy remains rare in animals. In this study we present a unique, stable and high-level heteroplasmy in male and female flies belonging to the neotropical Drosophila paulistorum species complex. We show that mitochondria of D. paulistorum...
Biased mutation spectra are pervasive, with widely varying direction and magnitude of mutational bias. Why are unbiased spectra rare, and how do such diverse biases evolve? We find that experimentally changing the mutation spectrum increases the beneficial mutation supply, because populations sample mutational classes that were poorly explored by the ancestor. Simulations show that selection does not oppose the evolution of a mutational bias in an unbiased ancestor; but it favours changing the direction...
Interspecific crossing experiments have shown that sex chromosomes play a major role in the reproductive isolation of many species. However, their ability to act as reproductive barriers, which hamper interspecific genetic exchange, has rarely been evaluated quantitatively compared to autosomes. However, this genome-wide limitation of gene flow is essential for understanding the complete separation of species, and thus speciation. Here, we develop a mainland-island model of secondary contact between...
Landmark-based geometric morphometrics has emerged as an essential discipline for the quantitative analysis of size and shape in ecology and evolution. With the ever-increasing density of digitized landmarks, the possible development of a fully automated method of landmark placement has attracted considerable attention. Despite the recent progress in image registration techniques, which could provide a pathway to automation, three-dimensional morphometric data is still mainly gathered by trained...
Computational analyses of pathogen genomes are increasingly used to unravel the dispersal history and transmission dynamics of epidemics. Here, we show how to go beyond historical reconstructions and use spatially-explicit phylogeographic and phylodynamic approaches to formally test epidemiological hypotheses. We illustrate our approach by focusing on the West Nile virus (WNV) spread in North America that has been responsible for substantial impacts on public, veterinary, and wildlife health. WNV...
Human centromeres form over arrays of tandemly repeated DNA that are exceptionally complex (repeats of repeats) and long (spanning up to 8 Mbp). They also have an exceptionally rapid rate of evolution. The generally accepted model for the expansion/contraction, homogenization and evolution of human centromeric repeat arrays is a generic model for the evolution of satellite DNA that is based on unequal crossing over between sister chromatids. This selectively neutral model predicts that the sequences...
Transparency reduces prey detectability by predators. While the proportion of transmitted light in aquatic species is higher as light availability increases, less is known about such variation in terrestrial species. Transparency has evolved several times in the typically opaque winged Lepidoptera order (moths and butterflies), displaying a large diversity of degrees. Using two complementary approaches, we explore how the evolution of the differences in light transmittance relates to habitat openness,...
Every species experiences limits to its geographic distribution. Some evolutionary models predict that populations at range edges are less well-adapted to their local environments due to drift, expansion load, or swamping gene flow from the range interior. Alternatively, populations near range edges might be uniquely adapted to marginal environments. In this study, we use a database of transplant studies that quantify performance at broad geographic scales to test how local adaptation, site quality,...
Setosphaeria turcica is a major fungal pathogen of maize and causes the foliar disease Northern corn leaf blight (NCLB). It originates from tropical regions and expanded into Central Europe since the 1980s, simultaneously with a rapid increase of maize cultivation area in this region. To investigate evolutionary processes influencing the rapid expansion of S. turcica we sequenced 121 isolates from Central Europe, Western Europe and Kenya. Population genetic inference revealed five genetically distinct...
Discrepancies in mitochondrial and nuclear genetic data are often interpreted as evidence of hybridisation. We re-examined reports of hybridisation in three cryptic stingless bee species in the genus Tetragonula in South East Queensland, Australia (T. carbonaria, T. davenporti, and T. hockingsi). Previous studies on this group using microsatellite markers proposed that occasional hybrids are found. In contrast, we find that allele frequencies at neutral regions of the nuclear genome, both microsatellites...
Studies in a variety of species have shown evidence for positively selected variants introduced into one population via introgression from another, distantly related population--a process known as adaptive introgression. However, there are few explicit frameworks for jointly modelling introgression and positive selection, in order to detect these variants using genomic sequence data. Here, we develop an approach based on convolutional neural networks (CNNs). CNNs do not require the specification...
The Central Highland Plateau of Madagascar is largely composed of grassland savanna, interspersed with patches of closed-canopy forest. Conventional wisdom has it that these grasslands are anthropogenic in nature, having been created very recently via human agricultural practices. Yet, the ancient origins of the endemic grasses suggest that the extensive savannas are natural biomes, similar to others found around the globe. We use a phylogeographic approach to compare these two competing scenarios....
Trait evolution in a set of species--a central theme in evolutionary biology--has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently...
The steps of sex chromosome evolution are often thought to follow a predictable pattern and tempo, but few studies have examined how the outcomes of this process differ between closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and Japan Sea stickleback (G. nipponicus) have been well characterized. Little is known, however, about the sex chromosomes in their distantly related congener, the blackspotted stickleback (G....
Genome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods. We studied synaptonemal complexes (SC) and prophase I processes in 44-chromosome intraspecific (Ellobius tancrei x E. tancrei) and interspecific (Ellobius talpinus x E. tancrei) hybrid mole voles heterozygous...
Biomedical and clinical sciences are experiencing a renewed interest in the fact that males and females differ in many anatomic, physiological, and behavioral traits. Sex differences in trait variability, however, are yet to receive similar recognition. In medical science, mammalian females are assumed to have higher trait variability due to estrous cycles (the estrus-mediated variability hypothesis); historically in biomedical research, females have been excluded for this reason. Contrastingly,...
Human-driven habitat fragmentation and loss have led to a proliferation of small and isolated plant and animal populations with high risk of extinction. One of the main threats to extinction in these populations is inbreeding depression, which is primarily caused by the exposure of recessive deleterious mutations as homozygous by inbreeding. The typical approach for managing these populations is to maintain high genetic diversity, often by translocating individuals from large populations to initiate...
Human sleep is linked with nearly every aspect of our health and wellbeing. The question whether and to what extent human sleep is in a state of evolutionary mismatch has gained recent attention from both clinical and biological science researchers. Here, I use a comparative Bayesian approach aimed at testing the sleep epidemic hypothesis - the idea that, due to labor demands and technological disruption, sleep-wake activity is negatively impacted in post-industrial, economically developed societies....
The three anterior-most segments in arthropods contain the ganglia that make up the arthropod brain. These segments, the pre-gnathal segments, are known to exhibit many developmental differences to other segments, believed to reflect their divergent morphology. We have analyzed the expression and function of the genes involved in the segment-polarity network in the pre-gnathal segments compared with the trunk segments in the hemimetabolous insect Oncopeltus fasciatus. We show that there are fundamental...
The paradox of stasis - the unexpectedly slow evolution of heritable traits under direct selection - has been widely documented in the last few decades. This paradox is often particularly acute for body size, which is often heritable and where positive associations of size and fitness are frequently identified, but constraints to the evolution of larger body sizes are often not obvious. Here, we identify a trade-off between survival and size-dependent reproduction in Soay sheep (Ovis aries), contributes...
The kinetic skull is a key innovation that allowed snakes to capture, manipulate, and swallow prey exclusively using their heads using the coordinated movement of 8 bones. Despite these unique feeding behaviors, patterns of evolutionary integration and modularity within the feeding bones of snakes in a phylogenetic framework have yet to be addressed. Here, we use a dataset of 60 {micro}CT scanned skulls and high-density geometric morphometric methods to address the origin and patterns of variation...
In contrast to the many theoretical studies on the adaptation of plant pathogens to qualitative resistances, few studies have investigated how quantitative resistance selects for increased pathogen aggressiveness. We formulate an integro-differential model with nonlocal effects of mutations to describe the evolutionary epidemiology dynamics of spore-producing pathogens in heterogeneous agricultural environments sharing a well-mixed pool of spores. Parasites reproduce clonally and each strain is characterized...
Disruption of placental gene expression contributes to several congenital developmental disorders in humans, and may play an important role in the evolution of reproductive barriers between species. The placenta is also highly enriched for interacting genes showing parent-of-origin or imprinted expression, which is thought to have evolved to mitigate parental conflict within this extra-embryonic tissue. However, relatively little is known about the broader organization, functional integration, and...
The evolution of mate preferences may depend on natural selection acting on the mating cues and on the underlying genetic architecture. While the evolution of assortative mating with respect to locally adapted traits has been well-characterized, the evolution of disassortative mating is poorly characterized. Here we aim at understanding the evolution of disassortative mating for traits under strong balancing selection, by focusing on polymorphic mimicry as an illustrative example. Positive frequency-dependent...
Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates where males are thus far unknown. Contrary to expectations, we find a diverse range...
The zoosporic obligate endoparasites, Olpidium, hold a pivotal position to the reconstruction of the flagellum loss in fungi, one of the key morphological transitions associated with the colonization of land by the early fungi. We generated genome and transcriptome data from non-axenic zoospores of Olpidium bornovanus and used a metagenome approach to extract phylogenetically informative fungal markers. Our phylogenetic reconstruction strongly supported Olpidium as the closest zoosporic relative...
In a context of ongoing biodiversity erosion, obtaining genomic resources from wildlife is becoming essential for conservation. The thousands of yearly mammalian roadkill could potentially provide a useful source material for genomic surveys. To illustrate the potential of this underexploited resource, we used roadkill samples to sequence reference genomes and study the genomic diversity of the bat-eared fox (Otocyon megalotis) and the aardwolf (Proteles cristata) for which subspecies have been defined...
The European sea bass (Dicentrarchus labrax) exhibits female-biased sexual size dimorphism (SDD) early in development. New tagging techniques provide the opportunity to monitor individual sex-related growth during the post-larval and juvenile stages. We produced an experimental population through artificial fertilization and followed a rearing-temperature protocol ([~]16 {degrees}C from hatching to 112 days post-hatching, dph; [~]20 {degrees}C from 117 to 358 dph) targeting a roughly balanced...
Studies of food microorganism domestication can provide important insight into adaptation mechanisms and lead to commercial applications. The Penicillium roqueforti fungus consists of four genetically differentiated populations, two of which have been domesticated for blue cheese-making, the other two thriving in other environments. Most blue cheeses are made with strains from a single P. roqueforti population, whereas Roquefort cheeses are inoculated with strains from a second population. We made...
Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to environmental variation. The importance of phenotypic plasticity in natural populations and its contribution to phenotypic evolution during rapid environmental change is widely debated. Here, we show that thermal plasticity of gene expression in natural populations is a key component of its adaptation: evolution to novel thermal environments increases ancestral plasticity rather than mean genetic...
Animal domestication typically affected numerous polygenic quantitative traits, such as behavior, development and reproduction. However, uncovering the genetic basis of quantitative trait variation is challenging, since they are caused by small allele-frequency changes. To date, only a few causative mutations related to domestication processes have been reported, strengthening the hypothesis that small effect variants have a prominent role. So far, approaches on domestication have been limited to...
Genetic drift is a basic evolutionary principle describing random changes in allelic frequencies with far-reaching consequences in various topics ranging from species conservation efforts to speciation. The conventional approach is to assume that genetic drift has the same effect on all populations undergoing the same change in size, regardless of the different behavior and history of the populations. However, here we reason that a simple act of learning from experience can significantly mitigate...
The antiviral innate immunity in mammals has evolved very rapidly in response to pathogen selective pressure. Studying the evolutionary diversification of mammalian antiviral defenses is of main importance to better understand our innate immune repertoire. The small HERC proteins are part of a multigene family including interferon-inducible antiviral effectors. Notably, HERC5 inhibits divergent viruses through the conjugation of ISG15 to diverse proteins-termed as ISGylation. Though HERC6 is the...
Point 1Phylodynamic models use pathogen genome sequence data to infer epidemiological dynamics. With the increasing genomic surveillance of pathogens, especially amid the SARS-CoV-2 outbreak, new practical questions about their use are emerging. Point 2One such question focuses on the inclusion of un-sequenced case occurrence data alongside sequenced data to improve phylodynamic analyses. This approach can be particularly valuable if sequencing efforts vary over time. Point 3Using simulations,...
Acoustic signaling by fishes has been recognized for millennia, but is typically regarded as comparatively rare within ray-finned fishes; as such, it has yet to be integrated into broader concepts of vertebrate evolution. We map the most comprehensive data set of volitional sound production of ray-finned fishes (Actinopterygii) yet assembled onto a family level phylogeny of the group, a clade representing more than half of extant vertebrate species. Our choice of family-level rather than species-level...
Across the Tree of Life (ToL), the complexity of proteomes varies widely. Our systematic analysis depicts that from the simplest archaea to mammals, the total number of proteins per proteome expanded ~200-fold. Individual proteins also became larger, and multi-domain proteins expanded ~50-fold. Apart from duplication and divergence of existing proteins, completely new proteins were born. Along the ToL, the number of different folds expanded ~5-fold and fold-combinations ~20-fold. Proteins prone to...
Closely related species with parapatric elevational ranges are ubiquitous in tropical mountains worldwide. The gradient speciation hypothesis proposes that these series are the result of in situ ecological speciation driven by divergent selection across elevation. Direct tests of this scenario have been hampered by the difficulty inferring the geographic arrangement of populations at the time of divergence. In cichlids, sticklebacks, and Timema stick insects, support for ecological speciation driven...
In bi-parental species, reproduction is not only a crucial life-history stage where individuals must take fitness-relevant decisions, but these decisions also need to be adjusted to the behavioural strategies of a partner. Hence, communication is required, which could be facilitated by condition-dependent signals of parental quality. Yet, these traits have (co-)evolved in multiple contexts within the family, as during reproduction different family members may coincide and interact at the site of...
Proteins are the workhorses of the cell, yet they carry great potential for harm via misfolding and aggregation. Despite the dangers, proteins are sometimes born de novo from non-coding DNA. Proteins are more likely to be born from non-coding regions that produce peptides that do little to no harm when translated than from regions that produce harmful peptides. To investigate which newborn proteins are most likely to "first, do no harm", we estimate fitnesses from an experiment that competed Escherichia...
AimThe evolutionary causes of the latitudinal diversity gradient are debated. Hypotheses have ultimately invoked either faster rates of diversification in the tropics, or more time for diversification due to the tropical origins of higher taxa. Here we perform the first test of the diversification rate and time hypotheses in freshwater ray-finned fishes, a group comprising nearly a quarter of all living vertebrates. LocationGlobal. Time period368-0 mya. Major taxa studiedExtant freshwater...
One of the most celebrated textbook examples of physiological adaptations to desert environments is the unique ability that desert mammals have to produce hyperosmotic urine. Commonly perceived as an adaptation mainly observed in small rodents, the extent to which urine concentrating ability has independently evolved in distinct lineages, including medium-sized and large desert mammals, has not previously been assessed using modern phylogenetic approaches. Here, we explicitly test the general hypothesis...
Gene duplication is an important source of evolutionary innovation, but the adaptive division-of-labor between duplicates can be opposed by ongoing gene conversion between them. Here we document a tandem duplication of Na+,K+-ATPase subunit 1 (ATP1A1) shared by frogs in the genus Leptodactylus, a group of species that feeds on toxic toads. One ATP1A1 paralog evolved resistance to toad toxins while the other paralog retained ancestral susceptibility. We show that the two Leptodactylus paralogs are...
A bacteriums fitness relative to its competitors, both in the presence and absence of antibiotics, plays a key role in its ecological success and clinical impact. In this study, we examine whether tetracycline-resistant mutants are less fit in the absence of the drug than their sensitive parents, and whether the fitness cost of resistance is constant or variable across independently derived lines. Tetracycline-resistant lines suffered, on average, a reduction in fitness of almost 8%. There was substantial...
In mammals, the placenta mediates maternal-fetal nutrient and waste exchange and provides immunomodulatory actions that facilitate maternal-fetal tolerance. The placenta is highly diversified among mammalian species, yet the molecular mechanisms that distinguish the placenta of human from other mammals are not fully understood. Using an interspecies transcriptomic comparison of human, macaque, and mouse term placentae, we identified hundreds of genes with lineage-specific expression - including dozens...
Recombination has been shown to contribute to HIV-1 evolution in vivo, but the underlying dynamics are extremely complex, depending on the nature of the fitness landscapes and of epistatic interactions. A less well-studied determinant of recombinant evolution is the mode of virus transmission in the cell population. HIV-1 can spread by free virus transmission, resulting largely in singly infected cells, and also by direct cell-to-cell transmission, resulting in the simultaneous infection of cells...
Many ideas about the evolution of specialization rely on trade-offs--an inability for one organism to express maximal performance in two or more environments. However, optimal foraging theory suggests that populations can evolve specialization on a superior resource without explicit trade-offs. Classical results in population genetics show that the process of adaptation can be biased toward further improvement in already productive environments, potentially widening the gap between superior and inferior...
The phenomenon of a massive vertebral deformity was recorded in the radiating Labeobarbus assemblage from the middle reaches of the Genale River (south-eastern Ethiopia, East Africa). Within this sympatric assemblage, five trophic morphs - generalized, lipped, piscivorous and two scraping feeders - were reported between 1993 and 2019. In 2009, a new morph with prevalence of [~]10% was discovered. The new morph, termed short, had an abnormally shortened vertebral column and a significantly heightened...
X chromosome inactivation (XCI) mediated by differential DNA methylation between sexes is well characterized in eutherian mammals. Although XCI is shared between eutherians and marsupials, the role of DNA methylation in marsupial XCI remains contested. Here we examine genome-wide signatures of DNA methylation from methylation maps across fives tissues from a male and female koala (Phascolarctos cinereus) and present the first whole genome, multi-tissue marsupial "methylome atlas." Using these novel...
Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers [NEW RESULTS]
Under the selfish centromere model, costs associated with female meiotic drive by centromeres select on interacting kinetochore proteins to restore Mendelian inheritance. We directly test this model in yellow monkeyflowers (Mimulus guttatus), which are polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. Quantitative genetic analyses reveal that variation in the strength...
Cells may be able to promote adaptive evolution in a gene-specific and temporally-controlled manner. Genes encoded on the lagging strand have a higher mutation rate and evolve faster than genes on the leading strand. This effect is likely driven by head-on replication-transcription conflicts, which occur when lagging strand genes are transcribed during DNA replication. We previously suggested that the ability to selectively increase mutagenesis in a subset of genes may provide an adaptive advantage...
Current procedures for inferring population history are generally performed under the assumption of complete neutrality - that is, by neglecting both direct selection and the effects of selection on linked sites. We here examine how the presence of direct purifying and background selection may bias demographic inference by evaluating two commonly-used methods (MSMC and fastsimcoal2), specifically studying how the underlying shape of the distribution of fitness effects (DFE) and the fraction of directly...
Climate change is predicted to increase the severity of environmental perturbations, including storms and droughts, which act as strong selective agents. These extreme events are often of finite duration (pulse disturbances). Hence, while evolution during an extreme event may be adaptive, the resulting phenotypic changes may become maladaptive when the event ends. Using individual-based models and analytic approximations that fuse quantitative genetics and demography, we explore how heritability...
Sex dimorphisms are widespread in animals and plants, for morphological as well as physiological traits. Understanding the genetic basis of sex dimorphism and its evolution is crucial for understanding biological differences between the sexes. Genetic variants with sex-antagonistic effects on fitness are expected to segregate in populations at the early phases of sexual dimorphism emergence. Detecting such variants is notoriously difficult, and the few genome-scan methods employed so far have limited...
The field of phylogeography has evolved rapidly in terms of the analytical toolkit to analyze the ever-increasing amounts of genomic data. Despite substantial advances, researchers have not fully explored all potential analytical tools to tackle the challenge posed by the huge size of genomic datasets. For example, deep learning techniques, such as convolutional neural networks (CNNs), widely employed in image and video classification, are largely unexplored for phylogeographic model selection. In...
After admixture, recombination breaks down genomic blocks of contiguous ancestry. The break down of these blocks forms a new molecular clock, that ticks at a much faster rate than the mutation clock, enabling accurate dating of admixture events in the recent past. However, existing theory on the break down of these blocks, or the accumulation of delineations between blocks, so called junctions, has been limited to using regularly spaced markers on phased data. Here, we present an extension to the...
O_LIThe rise of globalization has spread organisms beyond their natural range, allowing further opportunity for introduced species to adapt to novel environments and potentially become aggressive invaders. Yet, the role of niche evolution in promoting the success of invasive species remains poorly understood. Here, we use thermal performance curves (TPCs) to test the following hypotheses about thermal adaptation during the invasion process. First, in response to strong selection from novel temperature...
The rate at which plants grow is a major functional trait in plant ecology. However, little is known about its evolution in natural populations. Here, we investigate evolutionary and environmental factors shaping variation in the growth rate of Arabidopsis thaliana. We used plant diameter as a proxy to monitor plant growth over time in environments that mimicked latitudinal differences in the intensity of natural light radiation, across a set of 278 genotypes sampled within four broad regions, including...
Parental care is a key component of an organisms reproductive strategy that is thought to trade-off with allocation towards immunity. Yet it is unclear how caring parents respond to pathogens: do infected parents reduce their amount of care as a sickness behaviour or simply from being ill, or do they prioritise their offspring by maintaining high levels of care? Here we explored the consequences of infection by the pathogen Serratia marcescens on mortality, time spent providing care, reproductive...
Methionine adenosyltransferase (MAT), which catalyzes the biosynthesis of S-adenosylmethionine from L-methionine and ATP, is an ancient, highly conserved enzyme present in all three domains of life. Although the MAT enzymes of each domain are believed to share a common ancestor, the sequences of archaeal MATs show a high degree of divergence from the sequences of bacterial and eukaryotic MATs. However, the structural and functional consequences of this sequence divergence are not well understood....
The risk of developing cancer is correlated with body size and lifespan within species. Between species, however, there is no correlation between cancer and either body size or lifespan, indicating that large, long-lived species have evolved enhanced cancer protection mechanisms. Elephants and their relatives (Proboscideans) are a particularly interesting lineage for the exploration of mechanisms underlying the evolution of augmented cancer resistance because they evolved large bodies recently within...
Current novel coronavirus disease (COVID-19) has spread globally within a matter of months. The virus establishes a success in balancing its deadliness and contagiousness, and causes substantial differences in susceptibility and disease progression in people of different ages, genders and pre-existing comorbidities. Since these host factors are subjected to epigenetic regulation, relevant analyses on some key genes underlying COVID-19 pathogenesis were performed to longitudinally decipher their epigenetic...
Island populations are hallmarks of extreme phenotypic evolution. Radical changes in resource availability and predation risk accompanying island colonization drive changes in behavior, which Darwin likened to tameness in domesticated animals. Although many examples of animal boldness are found on islands, the heritability of observed behaviors, a requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety and exploration in island and mainland inbred strains of house...
In many yeast species the three genes at the center of the galactose catabolism pathway, GAL1, GAL10 and GAL7, are neighbors in the genome and form a metabolic gene cluster. We report here that some yeast strains in the genus Torulaspora have much larger GAL clusters that include genes for melibiase (MEL1), galactose permease (GAL2), glucose transporter (HGT1), phosphoglucomutase (PGM1), and the transcription factor GAL4, in addition to GAL1, GAL10, and GAL7. Together, these 8 genes encode almost...
Many parasites with complex life cycles modify their intermediate hosts behaviour, presumably to increase transmission to their final host. The threespine stickleback (Gasterosteus aculeatus) is an intermediate host in the cestode Schistocephalus solidus life cycle, which ends in an avian host, and shows increased risky behaviours when infected. We studied brain gene expression profiles of sticklebacks infected with S.solidus to determine the proximal causes of these behavioural alterations. We show...
A common question that arises when inferring species-level phylogenies from genome-scale data is whether selection acting on certain parts of the genome could create a bias in the inferred phylogeny. While most methods for species tree inference currently assume the multispecies coalescent (MSC), all methods that we are aware of utilize only the neutral coalescent process. If selection is in fact present, failure to adequately model it could introduce substantial bias. We work toward rigorously addressing...
How can a self-organized cellular function evolve, adapt to perturbations, and acquire new sub-functions? To make progress in answering these basic questions of evolutionary cell biology, we analyze, as a concrete example, the cell polarity machinery of Saccharomyces cerevisiae. This cellular module exhibits an intriguing resilience: it remains operational under genetic perturbations and recovers quickly and reproducibly from the deletion of one of its key components. Using a combination of modeling,...
Gene mutations endowing herbicide resistance may have negative pleiotropic effects on plant fitness. Quantifying these effects is critical for predicting the evolution of herbicide resistance and developing management strategies for herbicide-resistant weeds. This study reports the effects of the acetohydroxyacid synthase (AHAS) Trp574Leu mutation throughout the life cycle of the weed feral radish (Raphanus sativus L.). Resistant and susceptible biotypes responded differently to light and water treatments...
Life-history trade-offs between the number and size of offspring produced, and the costs of reproduction on future reproduction and survival can all be affected by different levels of parental effort. Because of these trade-offs the parents and the offspring have different optima for the amount of care given to the current brood, which leads to a conflict between parents and offspring. The offspring, as well as the parents, have the ability to affect parental effort, and thus changes in offspring...
AO_SCPLOWBSTRACTC_SCPLOWParasites can select for sexual reproduction in host populations, preventing replacement by faster growing asexual lineages. This is usually attributed to so-called "Red Queen Dynamics" (RQD), where antagonistic coevolution causes fluctuating selection in allele frequencies, which provides sex with an advantage over asex. However, parasitism may also maintain sex in the absence of RQD when sexual populations are more genetically diverse - and hence more resistant, on average...
Chance, contingency, and necessity in the experimental evolution of ancestral proteins [NEW RESULTS]
The extent to which chance and contingency shaped the sequence outcomes of protein evolution is largely unknown. To directly characterize the causes and consequences of chance and contingency, we combined directed evolution with ancestral protein reconstruction. By repeatedly selecting a phylogenetic series of ancestral proteins in the B-cell lymphoma-2 family to evolve the same protein-protein interaction specificities that existed during history, we show that contingency and chance interact to...
One of the central problems of vertebrate evolution is understanding the relationship among the distal portions of fins and limbs. Lacking comparable morphological markers of these regions in fish and tetrapods, these relationships have remained uncertain for the past century and a half. Here we show that Gli3 functions in controlling the proliferative expansion of distal progenitors are shared among median and paired fins as well as tetrapod limbs. Mutant knockout gli3 fins in medaka (Oryzias latipes)...
Antagonistic interactions are widespread in the microbial world and affect microbial evolutionary dynamics. Natural microbial communities often display spatial structure, which affects biological interactions, but much of what we know about microbial warfare comes from laboratory studies of well-mixed communities. To overcome this limitation, we manipulated two killer strains of the budding yeast Saccharomyces cerevisiae, expressing different toxins, to independently control the rate at which they...
In most species, natural selection plays a key role in genomic heterogeneous divergence. Additionally, barriers to gene flow, such as chromosomal rearrangements or gene incompatibilities, can cause genome heterogeneity. We used genome-wide re-sequencing data from 27 Populus alba and 28 P. adenopoda individuals to explore the causes of genomic heterogeneous differentiation in these two closely related species. In highly differentiated regions, neutrality tests (Tajimas D and Fay & Wus H) revealed...
Actinopterygians (ray-finned fishes) are the most diversified group of vertebrates and are characterized by a variety of protective structures covering their tegument, the evolution of which has intrigued biologists for decades. Paleontological records showed that the first mineralized vertebrate skeleton was composed of dermal bony plates covering the body, including odontogenic and skeletogenic components. Later in evolution, the exoskeleton of actinopterygians trunk was composed of scale structures....
Elucidating the timescale of evolution of bacteria is key to testing hypotheses on their co-evolution with eukaryotic hosts, which, however, is largely limited by the scarcity of bacterial fossils. Here, we incorporate eukaryotic fossils to date the divergence times of Alphaproteobacteria, based on the endosymbiosis theory that mitochondria evolved from an alphaproteobacterial lineage. We estimate that Alphaproteobacteria arose ~1900 million years (Ma) ago, followed by rapid divergence of their major...
Although tRNA structure is one of the most conserved and recognizable shapes in molecular biology, aberrant tRNAs are frequently found in the mitochondrial genomes of metazoans. The structure of several mitochondrial tRNAs is so degenerate that doubts have been raised about their expression and function. Mites from the arachnid superorder Acariformes are predicted to have some of the shortest mitochondrial tRNAs, with apparent base mismatches in acceptor stems and a complete loss of cloverleaf-life...
Because sensory signals often evolve rapidly, they could be instrumental in the emergence of reproductive isolation between species. However, pinpointing their specific contribution to isolating barriers, and the mechanisms underlying their divergence, remains challenging. Here we demonstrate sexual isolation due to divergence in chemical signals between members of the Drosophila americana group, dissect its underlying phenotypic and genetic mechanisms, and propose a model of its evolutionary history....
Eusocial animals often achieve ecological dominance in the ecosystems where they occur, a process that may be linked to their demography. That is, reproductive division of labor and high reproductive skew in eusocial species is predicted to result in more stable effective population sizes that may make groups more competitive, but also lower effective population sizes that may make groups more susceptible to inbreeding and extinction. We examined the relationship between demography and social organization...
Strict endosymbiont bacteria with high degree of genome reduction retain smaller proteins and, in certain cases, lack complete functional domains compared to their free-living counterparts. Until now, the mechanisms underlying these genetic reductions are not well understood. However, it is thought that, in order to compensate for gene reduction, somehow hosts take over those vital functions that endosymbionts cannot perform. In the present study, the conservation of RNA polymerases, the essential...
Whole genome sequences and coalescence theory allow the study of plant evolution in unprecedented detail. In this study we extend the genomic resources for the wild Mediterranean grass Brachypodium distachyon to investigate the scale of population structure and its underlying history at whole-genome resolution. The analysis of 196 accessions, spanning the Mediterranean from Iberia to Iraq, shows that the interplay of high selfing and seed dispersal rates has shaped genetic structure. At the continental...
Estimates of marine plastic stocks, a major threat to marine life (1), are far lower than expected from exponentially-increasing litter inputs, suggesting important loss factors (2, 3). These may involve microbial degradation, as the plastic-degrading polyethylene terephthalate enzyme (PETase) has been reported in marine microbial communities (4). An assessment of 416 metagenomes of planktonic communities across the global ocean identifies 68 oceanic PETase variants (oPETase) that evolved from ancestral...
Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex-biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography and neutral processes which...
Inferences about past processes of adaptation and speciation require a gene-scale and genome-wide understanding of the evolutionary history of diverging taxa. In this study, we use genome-wide capture of nuclear gene sequences, plus skimming of organellar sequences, to investigate the phylogenomics of monkeyflowers in Mimulus section Erythranthe (27 accessions from seven species). Taxa within Erythranthe, particularly the parapatric and putatively sister species M. lewisii (bee-pollinated) and M....
Alternative spicing is an integral part of gene expression in multicellular organisms that allows for diverse mRNA transcripts and proteins to be produced from a single gene. However, most existing analyses have focused on macro-evolution, with only limited research on splice site evolution over shorter term, micro-evolutionary time scales. Here we examine splicing evolution that has occurred during domestication and observe 45 novel splice forms with strongly transgressive isoform compositions,...
Allopolyploidization, which involves hybridization and genome doubling, is a key driving force in higher plant evolution. The transcriptome reprogramming that accompanies allopolyploidization can cause extensive phenotypic variations, and thus confers allopolyploids higher evolutionary potential than their diploid progenitors. Despite many studies, little is known about the interplay between hybridization and genome doubling in transcriptome reprogramming during allopolyploidization. Here, we performed...
The novel Coronavirus from Wuhan China discovered in December 2019 (nCOV-2019) has since developed into a global epidemic with major concerns about the possibility of the virus evolving into something even more sinister. In the present study we constructed the phylo-geo-network of nCOV-2019 genomes from across India to understand the viral evolution in the country. A total of 611 full length genomes were extracted from different states of India from the EpiCov repository of GISAID initiative and...
Understanding the conservation and evolution of protein complexes is of critical value to decode their function in physiological and pathological processes. One prominent proposal posits gene duplication as a potential mechanism for protein complex evolution. In this study we take advantage of large-scale proteome expression datasets to systematically investigate the role of paralogues, and specifically self-interacting paralogues, in shaping the evolutionary trajectories of protein complexes. First,...
Founder events play a critical role in shaping genetic diversity, impacting the fitness of a species and disease risk in humans. Yet our understanding of the prevalence and distribution of founder events in humans and other species remains incomplete, as most existing methods for characterizing founder events require large sample sizes or phased genomes. To learn about the frequency and evolutionary history of founder events, we introduce ASCEND (Allele Sharing Correlation for the Estimation of Non-equilibrium...
Colouration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected colouration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes...
In previous papers in this series, I described the "evolutionary genetic species concept" which is based on population genetic theory and should be applicable to any organism. I also described a species criterion, the K/{theta} ratio, that delimits independently evolving evolutionary species based on single-gene sequences. I then illustrated its application to sexual and asexual eukaryotes. Here, I show how the evolutionary genetic species concept and the K/{theta} ratio can be applied to bacteria,...
Domestication involves recent adaptation under strong human selection and rapid diversification, and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white mold Penicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole genome-based analyses of genetic relationships and diversity revealed that an ancient domestication...
AO_SCPLOWBSTRACTC_SCPLOWSex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex chromosome biology both from a functional (i.e. number of sex-linked genes) and evolutionary perspective (i.e. extent of Y degeneration and X-Y heteromorphy). The evolution of the pseudoautosomal boundary (PAB) - the limit between the recombining and the non-recombining regions of the sex...
Hmx gene conservation identifies the evolutionary origin of vertebrate cranial ganglia [NEW RESULTS]
The evolutionary origin of vertebrates included innovations in sensory processing associated with the acquisition of a predatory lifestyle1. Vertebrates perceive external stimuli through sensory systems serviced by cranial sensory ganglia (CSG) which develop from cranial placodes; however understanding the evolutionary origin of placodes and CSGs is hampered by the gulf between living lineages and difficulty in assigning homology between cell types and structures. Here we use the Hmx gene family...
The rate at which plants grow is a major functional trait in plant ecology. However, little is known about its evolution in natural populations. Here, we investigate evolutionary and environmental factors shaping variation in the growth rate of Arabidopsis thaliana. We used plant diameter as a proxy to monitor plant growth over time in environments that mimicked latitudinal differences in the intensity of natural light radiation, across a set of 278 genotypes sampled within four broad regions, including...
1An evolutionary process is reflected in the sequence of changes through time of any trait (e.g. morphological, molecular). Yet, a better understanding of evolution would be procured by characterizing correlated evolution, or when two or more evolutionary processes interact. A wide range of parametric methods have previously been proposed to detect correlated evolution but they often require significant computing time as they rely on the estimation of many parameters. Here we propose a minimal likelihood...
What determines genetic diversity and how it connects to the various biological traits is unknown. In this work, we offer answers to these questions. By comparing genetic variation of 14,671 mammalian gene trees with thousands of individual genomes of human, chimpanzee, gorilla, mouse and dog/wolf, we found that intraspecific genetic diversity is determined by long-term molecular evolutionary rates, rather than de novo mutation rates. This relationship was established during the early stage of mammalian...
While the majority of Drosophila species lay eggs onto fermented fruits, females of D. suzukii pierce the skin and lay eggs into ripening fruits using their serrated ovipositors. The changes of oviposition site preference must have accompanied this niche exploitation. In this study, we established an oviposition assay to investigate the effects of commensal microbes deposited by conspecific and heterospecific individuals, and showed that presence of microbes on the oviposition substrate enhances...
The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. Whilst it is clear that the current contact zones between sister taxa are secondary and have formed during the last interglacial, it is unclear when the taxa involved began to diverge. Previous estimates are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. We use genome-wide transcriptome data to estimate...
Environmental features can alter the behaviours and phenotypes of organisms and populations evolving within them including the dynamics between natural and sexual selection. Experimental environmental manipulation, particularly when conducted in experiments where the dynamics of the purging of deleterious alleles are compared, has demonstrated both direct and indirect effects on the strength and direction of selection. However, many of these experiments are conducted with fairly simplistic environments...
Eutherian (placental) mammals exhibit great differences in the degree of placental invasion into the maternal endometrium, with humans being on the most invasive end. Previously, we have shown that these differences in invasiveness is largely controlled by the stromal fibroblasts of the maternal endometrium, with secondary effect on stroma of other tissues resulting in correlated differences in cancer malignancy. Here, we present a statistical investigation of the second dogma linking the phenotypic...
Unraveling the origin of molecular pathways underlying the evolution of adaptive traits is essential for understanding how new lineages emerge, including the relative contribution of conserved, ancestral traits, and newly evolved, derived traits. Here, we investigated the evolutionary divergence of sex pheromone communication from moths (mostly nocturnal) to butterflies (mostly diurnal) that occurred ~98 million years ago. In moths, females typically emit pheromones to attract male mates, but in...
Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here we study the only presumed case of androdioecy in insects, found in the cottony cushion scale, Icerya purchasi. In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, rare males are sometimes observed too. In a large population-genetic analysis, we show for the first time that although self-fertilization...
Reticulate evolutionary events are hallmarks of plant phylogeny, and are increasingly recognized as common occurrences in other branches of the Tree of Life. However, inferring the evolutionary history of admixed lineages presents a difficult challenge for systematists due to genealogical discordance caused by both incomplete lineage sorting (ILS) and hybridization. Methods that accommodate both of these processes are continuing to be developed, but they often do not scale well to larger numbers...
X and Y chromosomes are usually derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution remain elusive. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X. To address this question, we quantified divergence between...
Given the importance of DNA methylation in protection of the genome against transposable elements and transcriptional regulation in other taxonomic groups, the diversity in both levels and patterns of DNA methylation in the insects raises questions about its function and evolution. We show that the maintenance DNA methyltransferase, DNMT1, affects meiosis and is essential to fertility in milkweed bugs, Oncopeltus fasciatus, while DNA methylation is not required in somatic cells. Our results support...
Many enveloped viruses such as HIV have evolved to transmit by two infection modes: cell-free infection and cell-to-cell spread. Cell-to-cell spread is highly efficient as it involves directed viral transmission from the infected to the uninfected cell. In contrast, cell-free infection relies on chance encounters between the virion and cell. Despite the higher efficiency of cell-to-cell spread, there is substantial transmission by cell-free infection in conjunction with cell-to-cell spread. A possible...
Insects and other arthropods utilise external sensory structures for mechanosensory, olfactory and gustatory reception. These sense organs have characteristic shapes related to their function, and in many cases are distributed in a fixed pattern so that they are identifiable individually. In Drosophila melanogaster, the identity of sense organs is regulated by specific combinations of transcription factors. In other arthropods, however, sense organ subtypes cannot be linked to the same code of gene...
Sponges live in symbioses with microbes that allow the hosts to exploit otherwise inaccessible resources. Given the potential of microbiomes to unlock new niche axes for the hosts, microbiomes may facilitate evolutionary innovation in the ecology of sponges. However, the hypothesis that ecological diversification evolves via the microbiome among multiple, closely related sponge species living in sympatry is yet untested. Here, we provide the first test of this hypothesis within Ircinia, a genus possessing...
Molecular analyses of closely related taxa have increasingly revealed the importance of higher-order genetic interactions in explaining the observed pattern of reproductive isolation between populations. Indeed, both empirical and theoretical studies have linked the process of speciation to complex genetic interactions. Gene Regulatory Networks (GRNs) capture the inter-dependencies of gene expression and encode information about an individuals phenotype and development at the molecular level. As...
Inferring the demographic history of species is one of the greatest challenges in populations genetics. This history is often represented as a history of size changes, thus ignoring population structure. Alternatively, structure is defined a priori as a population tree and not inferred. Here we propose a framework based on the IICR (Inverse Instantaneous Coalescence Rate), which can be estimated using the PSMC method of Li and Durbin (2011) for a single diploid individual. For an isolated population,...
Deeply divergent mitochondrial genomes can reveal hidden diversity within species, however robust assessments of diversity require corroborative divergence in the nuclear genome. Previous phylogeographic analysis of the Common Blue butterfly (Polyommatus icarus) revealed a deeply divergent mitotype in Europe. Here, we reconstruct the phylogeography of this butterfly in the British Isles using both mitochondrial and nuclear DNA. We found strong geographical structuring of three distinct CO1 mitotypes...
BackgroundWe compare life histories and selection forces among chimpanzees and human subsistence societies in order to identify the age-specific vital rates that best explain fitness variation, selection pressures and species divergence. MethodsWe employ Life Table Response Experiments that quantify vital rate contributions to population growth rate differences. Although widespread in ecology, these methods have not been applied to human populations or to look at species differences among humans...
Selection against severe mitochondrial mutations is facilitated by germline processes, lowering the risk of genetic diseases. How selection works is disputed: experimental data are conflicting and previous modelling work has not clarified the issues. Here we develop computational and evolutionary models that compare the outcome of selection at the level of individuals, cells and mitochondria. Using realistic de novo mutation rates and germline development parameters, the evolutionary model accurately...
Hybridization of closely related plant species is frequently connected to endosperm arrest and seed failure, for reasons that remain to be identified. In this study, we investigated the molecular events accompanying seed failure in hybrids of the closely related species pair Capsella rubella and C. grandiflora. Mapping of QTLs for the underlying cause of hybrid incompatibility in Capsella revealed three QTLs that were close to pericentromeric regions. This prompted us to investigate whether there...
O_LIIn many species that fight over resources, individuals use specialized structures to overpower their rivals (i.e. weapons). Despite their similar roles for contest settlement (i.e. affecting the winning chances), weapons are highly diverse morphological structures across species. However, the comprehension on how this diversity evolved is still open for debate. C_LIO_LIUnfortunately, most studies on how weapons are used during contests focus on size asymmetries between winners and losers. Although...
The growing availability of genetic datasets, in combination with machine learning frameworks, offer great potential to answer long-standing questions in ecology and evolution. One such question has intrigued population geneticists, biogeographers, and conservation biologists: What determines intraspecific genetic diversity? This question is challenging to answer because many factors may influence genetic variation, including life history traits, historical influences, and geography, and the relative...
Organisms differ in the types and numbers of tRNA genes that they carry. While the evolutionary mechanisms behind tRNA gene set evolution have been investigated theoretically and computationally, direct observations of tRNA gene set evolution remain rare. Here, we report the evolution of a tRNA gene set in laboratory populations of the bacterium Pseudomonas fluorescens SBW25. The growth defect caused by deleting the single-copy tRNA gene, serCGA, is rapidly compensated by large-scale (45-290 kb)...
The vegetable ivory palms (Phytelepheae) form a small group of Neotropical palms whose phylogenetic relationships are not fully understood. Three genera and eight species are currently recognized; however, it has been suggested that Phytelephas macrocarpa could include the species Phytelephas seemannii and Phytelephas schottii because of supposed phylogenetic relatedness and similar morphology. We inferred their phylogenetic relationships and divergence time estimates using the 32 most clock-like...
The Bering Land Bridge connecting North America and Eurasia was periodically exposed and inundated by oscillating sea levels during the Pleistocene glacial cycles. This land connection allowed the intermittent dispersal of animals, including humans, between Western Beringia (far north-east Asia) and Eastern Beringia (north-west North America), changing the faunal community composition of both continents. The Pleistocene glacial cycles also had profound impacts on temperature, precipitation, and vegetation,...
Telomere length is correlated positively with longevity at the individual level, but negatively when compared across species. Here, we tested the association between lifespan and telomere length in African annual killifish. We analyzed telomere length in 18 Nothobranchius strains derived from diverse habitats and measured the laboratory lifespan of 14 strains of N. furzeri and N. kadleci. We found that males had shorter telomeres than females. The longest telomeres were recorded in strains derived...
There are two families of quantitative methods for inferring geographical homelands of language families: Bayesian phylogeography and the diversity method. Bayesian methods model how populations may have moved using the backbone of a phylogenetic tree, while the diversity method, which does not need a tree as input, is based on the idea that the geographical area where linguistic diversity is highest likely corresponds to the homeland. No systematic tests of the performances of the different methods...
Photosynthesis--both oxygenic and more ancient anoxygenic forms--has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding...
The relationship between microbiomes and selective regimes in the sponge genus Ircinia [NEW RESULTS]
Sponges are often densely populated by microbes that benefit their hosts through nutrition and bioactive secondary metabolites; however, sponges must simultaneously contend with the toxicity of microbes and thwart microbial overgrowth. Despite these fundamental tenets of sponge biology, the patterns of selection in the host sponges genomes that underlie tolerance and control of their microbiomes are still poorly understood. To elucidate these patterns of selection, we performed a population genetic...
Phenotypic plasticity, the ability of an organism to express multiple phenotypes in response to the prevailing environmental conditions without genetic change, may occur as a response to anthropogenic environmental change. Arguably, the most significant future anthropogenic environment change is contemporary climate change. Given that increasing climate variability is predicted to pose a greater risk than directional climate change, we tested the effect of a water temperature differential of 4 {o}C...
Cas9 trans-activating CRISPR RNAs (tracrRNAs) form distinct structures essential for target recognition and cleavage and dictate exchangeability between orthologous proteins. As non-coding RNAs that are often apart from the CRISPR array, their identification can be arduous. In this paper, a new bioinformatic method for the detection of Cas9 tracrRNAs is presented. The approach utilizes a co-variance model (CM) based on both sequence homology and predicted secondary structure to locate tracrRNAs....
Lifestyle convergences and related phenotypes are a major topic in evolutionary biology. Low bone cortical compactness (CC), shared by the two genera of tree sloths, has been linked to their convergently evolved slow arboreal ecology. The proposed relationship of low CC with tree sloths lifestyle suggests a potential convergent acquisition of this trait in other slow arboreal mammals. Tree sloths, Lorisidae, Palaeopropithecidae, Megaladapis and koalas were included in a phylogenetically informed...
AO_SCPLOWBSTRACTC_SCPLOWA central tenet of evolutionary theory is that it requires variation upon which selection can act. We describe a means of attaining cumulative, adaptive, open-ended change that requires neither variation nor selective exclusion, and that can occur in the absence of generations (i.e., no explicit birth or death). This second evolutionary process occurs through the assimilation, restructuring, and extrusion of products into the environment by identical, interacting Reflexively...
The microbiome can contribute to variation in fitness-related traits of their hosts, and thus to host evolution. Hosts are therefore expected to be under selection to control their microbiome, for instance through controlling microbe transmission from parents to offspring. Current models have mostly focused on microbes that either increase or decrease fitness. In that case, host-level selection is relatively straightforward, favouring either complete or no inheritance. In natural systems, however,...
Although the biomass of chum salmon (Oncorhynchus keta) in the North Pacific is at a historical maximum, the number of individuals returning to Japan, the location of the worlds largest chum salmon hatchery program, has declined substantially over 25 years. To search for potential causes of this decline, we synthesized catch/release, sea surface temperature (SST), and published genetic data, namely, microsatellites, single nucleotide polymorphisms collected for efficient stock identification, lactate...
Spatial and seasonal variation in the environment are ubiquitous. Environmental heterogeneity can affect natural populations and lead to covariation between environment and allele frequencies. Drosophila melanogaster is known to harbor polymorphisms that change both with latitude and seasons. Identifying the role of selection in driving these changes is not trivial, because non-adaptive processes can cause similar patterns. Given the environment changes in similar ways across seasons and along the...
AO_SCPLOWBSTRACTC_SCPLOWGene paralogs are copies of a same gene that appear after gene or full genome duplication. Redundancy generated by gene duplication may release certain evolutionary pressures, allowing one of the copies to access novel gene functions. Here we focused on role of codon usage preferences (CUPrefs) during the evolution of the polypyrimidine tract binding protein (PTBP) splicing regulator paralogs. PTBP1-3 show high identity at the amino acid level (up to 80%), but display...
Though seemingly bizarre, the dramatic post-embryonic transformation that occurs during metamorphosis is one of the most widespread and successful developmental strategies on the planet. The adaptive decoupling hypothesis (ADH) proposes that metamorphosis is an adaptation for optimizing expression of traits across life stages that experience opposing selection pressures. Similarly, sex-biased expression of traits is thought to evolve in response to sexually antagonistic selection. Both hypotheses...
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