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Molecular Biology and Evolution

How Algae Adapt to the Extreme Antarctic Cold

Mon, 24 Feb 2020 00:00:00 GMT

Typically, algae are known as the pond scum associated with extremely warm summer temperatures near the shores of lakes or oceans. Now, a new study shows that when they are shifted to the extreme cold of Antarctica, special antifreeze enzymes and proteins can kick into gear to help them adapt and survive.

Shark and Ray Vision Come into Focus

Mon, 24 Feb 2020 00:00:00 GMT

Vision is a crucial sense for most animals, and vertebrates have evolved a highly adaptable set of opsin genes that generate light-sensitive pigments to decode the retinal image. These opsins include a rod opsin to help see in low light, and four classes of cone opsins to see in bright light and detect colors across the visible light spectrum.

Estimating Pangenomes with Roary

Tue, 17 Dec 2019 00:00:00 GMT

Abstract
A description of the genetic makeup of a species based on a single genome is often insufficient because it ignores the variability in gene repertoire among multiple strains. The estimation of the pangenome of a species is a solution to this issue as it provides an overview of genes that are shared by all strains and genes that are present in only some of the genomes. These different sets of genes can then be analyzed functionally to explore correlations with unique phenotypes and adaptations. This protocol presents the usage of Roary, a Linux-native pangenome application. Roary is a straightforward software that provides 1) an overview about core and accessory genes for those interested in general trends and, also, 2) detailed information on gene presence/absence in each genome for in-depth analyses. Results are provided both in text and graphic format.

The Loci of Behavioral Evolution: Evidence That Fas2 and tilB Underlie Differences in Pupation Site Choice Behavior between Drosophila melanogaster and D. simulans

Wed, 27 Nov 2019 00:00:00 GMT

Abstract
The behaviors of closely related species can be remarkably different, and these differences have important ecological and evolutionary consequences. Although the recent boom in genotype–phenotype studies has led to a greater understanding of the genetic architecture and evolution of a variety of traits, studies identifying the genetic basis of behaviors are, comparatively, still lacking. This is likely because they are complex and environmentally sensitive phenotypes, making them difficult to measure reliably for association studies. The Drosophila species complex holds promise for addressing these challenges, as the behaviors of closely related species can be readily assayed in a common environment. Here, we investigate the genetic basis of an evolved behavioral difference, pupation site choice, between Drosophila melanogaster and D. simulans. In this study, we demonstrate a significant contribution of the X chromosome to the difference in pupation site choice behavior between these species. Using a panel of X-chromosome deficiencies, we screened the majority of the X chromosome for causal loci and identified two regions associated with this X-effect. We then collect gene disruption and RNAi data supporting a single gene that affects pupation behavior within each region: Fas2 and tilB. Finally, we show that differences in tilB expression correlate with the differences in pupation site choice behavior between species. This evidence associating two genes with differences in a complex, environmentally sensitive behavior represents the first step toward a functional and evolutionary understanding of this behavioral divergence.

Visual Opsin Diversity in Sharks and Rays

Tue, 26 Nov 2019 00:00:00 GMT

Abstract
The diversity of color vision systems found in extant vertebrates suggests that different evolutionary selection pressures have driven specializations in photoreceptor complement and visual pigment spectral tuning appropriate for an animal’s behavior, habitat, and life history. Aquatic vertebrates in particular show high variability in chromatic vision and have become important models for understanding the role of color vision in prey detection, predator avoidance, and social interactions. In this study, we examined the capacity for chromatic vision in elasmobranch fishes, a group that have received relatively little attention to date. We used microspectrophotometry to measure the spectral absorbance of the visual pigments in the outer segments of individual photoreceptors from several ray and shark species, and we sequenced the opsin mRNAs obtained from the retinas of the same species, as well as from additional elasmobranch species. We reveal the phylogenetically widespread occurrence of dichromatic color vision in rays based on two cone opsins, RH2 and LWS. We also confirm that all shark species studied to date appear to be cone monochromats but report that in different species the single cone opsin may be of either the LWS or the RH2 class. From this, we infer that cone monochromacy in sharks has evolved independently on multiple occasions. Together with earlier discoveries in secondarily aquatic marine mammals, this suggests that cone-based color vision may be of little use for large marine predators, such as sharks, pinnipeds, and cetaceans.

Early Stage Adaptation of a Mesophilic Green Alga to Antarctica: Systematic Increases in Abundance of Enzymes and LEA Proteins

Wed, 20 Nov 2019 00:00:00 GMT

Abstract
It is known that adaptive evolution in permanently cold environments drives cold adaptation in enzymes. However, how the relatively high enzyme activities were achieved in cold environments prior to cold adaptation of enzymes is unclear. Here we report that an Antarctic strain of Chlorella vulgaris, called NJ-7, acquired the capability to grow at near 0 °C temperatures and greatly enhanced freezing tolerance after systematic increases in abundance of enzymes/proteins and positive selection of certain genes. Having diverged from the temperate strain UTEX259 of the same species 2.5 (1.1–4.1) to 2.6 (1.0–4.5) Ma, NJ-7 retained the basic mesophilic characteristics and genome structures. Nitrate reductases in the two strains are highly similar in amino acid sequence and optimal temperature, but the NJ-7 one showed significantly higher abundance and activity. Quantitative proteomic analyses indicated that several cryoprotective proteins (LEA), many enzymes involved in carbon metabolism and a large number of other enzymes/proteins, were more abundant in NJ-7 than in UTEX259. Like nitrate reductase, most of these enzymes were not upregulated in response to cold stress. Thus, compensation of low specific activities by increased enzyme abundance appears to be an important strategy for early stage cold adaptation to Antarctica, but such enzymes are mostly not involved in cold acclimation upon transfer from favorable temperatures to near 0 °C temperatures.

Recurrent Collection of Drosophila melanogaster from Wild African Environments and Genomic Insights into Species History

Fri, 15 Nov 2019 00:00:00 GMT

Abstract
A long-standing enigma concerns the geographic and ecological origins of the intensively studied vinegar fly, Drosophila melanogaster. This globally distributed human commensal is thought to originate from sub-Saharan Africa, yet until recently, it had never been reported from undisturbed wilderness environments that could reflect its precommensal niche. Here, we document the collection of 288 D. melanogaster individuals from multiple African wilderness areas in Zambia, Zimbabwe, and Namibia. The presence of D. melanogaster in these remote woodland environments is consistent with an ancestral range in southern-central Africa, as opposed to equatorial regions. After sequencing the genomes of 17 wilderness-collected flies collected from Kafue National Park in Zambia, we found reduced genetic diversity relative to town populations, elevated chromosomal inversion frequencies, and strong differences at specific genes including known insecticide targets. Combining these genomes with existing data, we probed the history of this species’ geographic expansion. Demographic estimates indicated that expansion from southern-central Africa began ∼10,000 years ago, with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,400 years ago. This improved model of demographic history will provide an important resource for future evolutionary and genomic studies of this key model organism. Our findings add context to the history of D. melanogaster, while opening the door for future studies on the biological basis of adaptation to human environments.

Domestication of High-Copy Transposons Underlays the Wheat Small RNA Response to an Obligate Pathogen

Fri, 15 Nov 2019 00:00:00 GMT

Abstract
Plant genomes have evolved several evolutionary mechanisms to tolerate and make use of transposable elements (TEs). Of these, transposon domestication into cis-regulatory and microRNA (miRNA) sequences is proposed to contribute to abiotic/biotic stress adaptation in plants. The wheat genome is derived at 85% from TEs, and contains thousands of miniature inverted-repeat transposable elements (MITEs), whose sequences are particularly prone for domestication into miRNA precursors. In this study, we investigate the contribution of TEs to the wheat small RNA immune response to the lineage-specific, obligate powdery mildew pathogen. We show that MITEs of the Mariner superfamily contribute the largest diversity of miRNAs to the wheat immune response. In particular, MITE precursors of miRNAs are wide-spread over the wheat genome, and highly conserved copies are found in the Lr34 and QPm.tut-4A mildew resistance loci. Our work suggests that transposon domestication is an important evolutionary force driving miRNA functional innovation in wheat immunity.

Unbiased Estimation of Linkage Disequilibrium from Unphased Data

Thu, 14 Nov 2019 00:00:00 GMT

Abstract
Linkage disequilibrium (LD) is used to infer evolutionary history, to identify genomic regions under selection, and to dissect the relationship between genotype and phenotype. In each case, we require accurate estimates of LD statistics from sequencing data. Unphased data present a challenge because multilocus haplotypes cannot be inferred exactly. Widely used estimators for the common statistics r2 and D2 exhibit large and variable upward biases that complicate interpretation and comparison across cohorts. Here, we show how to find unbiased estimators for a wide range of two-locus statistics, including D2, for both single and multiple randomly mating populations. These unbiased statistics are particularly well suited to estimate effective population sizes from unlinked loci in small populations. We develop a simple inference pipeline and use it to refine estimates of recent effective population sizes of the threatened Channel Island Fox populations.

Somatic Mutations and Genome Stability Maintenance in Clonal Coral Colonies

Wed, 13 Nov 2019 00:00:00 GMT

Abstract
One challenge for multicellular organisms is maintaining genome stability in the face of mutagens across long life spans. Imperfect genome maintenance leads to mutation accumulation in somatic cells, which is associated with tumors and senescence in vertebrates. Colonial reef-building corals are often large, can live for hundreds of years, rarely develop recognizable tumors, and are thought to convert somatic cells into gamete producers, so they are a pivotal group in which to understand long-term genome maintenance. To measure rates and patterns of somatic mutations, we analyzed transcriptomes from 17 to 22 branches from each of four Acropora hyacinthus colonies, determined putative single nucleotide variants, and verified them with Sanger resequencing. Unlike for human skin carcinomas, there is no signature of mutations caused by UV damage, indicating either higher efficiency of repair than in vertebrates, or strong sunscreen protection in these shallow water tropical animals. The somatic mutation frequency per nucleotide in A. hyacinthus is on the same order of magnitude (10−7) as noncancerous human somatic cells, and accumulation of mutations with age is similar. Loss of heterozygosity variants outnumber gain of heterozygosity mutations ∼2:1. Although the mutation frequency is similar in mammals and corals, the preponderance of loss of heterozygosity changes and potential selection may reduce the frequency of deleterious mutations in colonial animals like corals. This may limit the deleterious effects of somatic mutations on the coral organism as well as potential offspring.

Developmental Systems Drift and the Drivers of Sex Chromosome Evolution

Mon, 11 Nov 2019 00:00:00 GMT

Abstract
Phenotypic invariance—the outcome of purifying selection—is a hallmark of biological importance. However, invariant phenotypes might be controlled by diverged genetic systems in different species. Here, we explore how an important and invariant phenotype—the development of sexually differentiated individuals—is controlled in over two dozen species in the frog family Pipidae. We uncovered evidence in different species for 1) an ancestral W chromosome that is not found in many females and is found in some males, 2) independent losses and 3) autosomal segregation of this W chromosome, 4) changes in male versus female heterogamy, and 5) substantial variation among species in recombination suppression on sex chromosomes. We further provide evidence of, and evolutionary context for, the origins of at least seven distinct systems for regulating sex determination among three closely related genera. These systems are distinct in their genomic locations, evolutionary origins, and/or male versus female heterogamy. Our findings demonstrate that the developmental control of sexual differentiation changed via loss, sidelining, and empowerment of a mechanistically influential gene, and offer insights into novel factors that impinge on the diverse evolutionary fates of sex chromosomes.

Ancient DNA Reconstructs the Genetic Legacies of Precontact Puerto Rico Communities

Sat, 09 Nov 2019 00:00:00 GMT

Abstract
Indigenous peoples have occupied the island of Puerto Rico since at least 3000 BC. Due to the demographic shifts that occurred after European contact, the origin(s) of these ancient populations, and their genetic relationship to present-day islanders, are unclear. We use ancient DNA to characterize the population history and genetic legacies of precontact Indigenous communities from Puerto Rico. Bone, tooth, and dental calculus samples were collected from 124 individuals from three precontact archaeological sites: Tibes, Punta Candelero, and Paso del Indio. Despite poor DNA preservation, we used target enrichment and high-throughput sequencing to obtain complete mitochondrial genomes (mtDNA) from 45 individuals and autosomal genotypes from two individuals. We found a high proportion of Native American mtDNA haplogroups A2 and C1 in the precontact Puerto Rico sample (40% and 44%, respectively). This distribution, as well as the haplotypes represented, supports a primarily Amazonian South American origin for these populations and mirrors the Native American mtDNA diversity patterns found in present-day islanders. Three mtDNA haplotypes from precontact Puerto Rico persist among Puerto Ricans and other Caribbean islanders, indicating that present-day populations are reservoirs of precontact mtDNA diversity. Lastly, we find similarity in autosomal ancestry patterns between precontact individuals from Puerto Rico and the Bahamas, suggesting a shared component of Indigenous Caribbean ancestry with close affinity to South American populations. Our findings contribute to a more complete reconstruction of precontact Caribbean population history and explore the role of Indigenous peoples in shaping the biocultural diversity of present-day Puerto Ricans and other Caribbean islanders.

Optimizing Phylogenomics with Rapidly Evolving Long Exons: Comparison with Anchored Hybrid Enrichment and Ultraconserved Elements

Sat, 09 Nov 2019 00:00:00 GMT

Abstract
Marker selection has emerged as an important component of phylogenomic study design due to rising concerns of the effects of gene tree estimation error, model misspecification, and data-type differences. Researchers must balance various trade-offs associated with locus length and evolutionary rate among other factors. The most commonly used reduced representation data sets for phylogenomics are ultraconserved elements (UCEs) and Anchored Hybrid Enrichment (AHE). Here, we introduce Rapidly Evolving Long Exon Capture (RELEC), a new set of loci that targets single exons that are both rapidly evolving (evolutionary rate faster than RAG1) and relatively long in length (>1,500 bp), while at the same time avoiding paralogy issues across amniotes. We compare the RELEC data set to UCEs and AHE in squamate reptiles by aligning and analyzing orthologous sequences from 17 squamate genomes, composed of 10 snakes and 7 lizards. The RELEC data set (179 loci) outperforms AHE and UCEs by maximizing per-locus genetic variation while maintaining presence and orthology across a range of evolutionary scales. RELEC markers show higher phylogenetic informativeness than UCE and AHE loci, and RELEC gene trees show greater similarity to the species tree than AHE or UCE gene trees. Furthermore, with fewer loci, RELEC remains computationally tractable for full Bayesian coalescent species tree analyses. We contrast RELEC to and discuss important aspects of comparable methods, and demonstrate how RELEC may be the most effective set of loci for resolving difficult nodes and rapid radiations. We provide several resources for capturing or extracting RELEC loci from other amniote groups.

Diet and Adaptive Evolution of Alanine-Glyoxylate Aminotransferase Mitochondrial Targeting in Birds

Fri, 08 Nov 2019 00:00:00 GMT

Abstract
Adaptations to different diets represent a hallmark of animal diversity. The diets of birds are highly variable, making them an excellent model system for studying adaptive evolution driven by dietary changes. To test whether molecular adaptations to diet have occurred during the evolution of birds, we examined a dietary enzyme alanine-glyoxylate aminotransferase (AGT), which tends to target mitochondria in carnivorous mammals, peroxisomes in herbivorous mammals, and both mitochondria and peroxisomes in omnivorous mammals. A total of 31 bird species were examined in this study, which included representatives of most major avian lineages. Of these, 29 have an intact mitochondrial targeting sequence (MTS) of AGT. This finding is in stark contrast to mammals, which showed a number of independent losses of the MTS. Our cell-based functional assays revealed that the efficiency of AGT mitochondrial targeting was greatly reduced in unrelated lineages of granivorous birds, yet it tended to be high in insectivorous and carnivorous lineages. Furthermore, we found that proportions of animal tissue in avian diets were positively correlated with mitochondrial targeting efficiencies that were experimentally determined, but not with those that were computationally predicted. Adaptive evolution of AGT mitochondrial targeting in birds was further supported by the detection of positive selection on MTS regions. Our study contributes to the understanding of how diet drives molecular adaptations in animals, and suggests that caution must be taken when computationally predicting protein subcellular targeting.

Phylogenomics Identifies an Ancestral Burst of Gene Duplications Predating the Diversification of Aphidomorpha

Fri, 08 Nov 2019 00:00:00 GMT

Abstract
Aphids (Aphidoidea) are a diverse group of hemipteran insects that feed on plant phloem sap. A common finding in studies of aphid genomes is the presence of a large number of duplicated genes. However, when these duplications occurred remains unclear, partly due to the high relatedness of sequenced species. To better understand the origin of aphid duplications we sequenced and assembled the genome of Cinara cedri, an early branching lineage (Lachninae) of the Aphididae family. We performed a phylogenomic comparison of this genome with 20 other sequenced genomes, including the available genomes of five other aphids, along with the transcriptomes of two species belonging to Adelgidae (a closely related clade to the aphids) and Coccoidea. We found that gene duplication has been pervasive throughout the evolution of aphids, including many parallel waves of recent, species-specific duplications. Most notably, we identified a consistent set of very ancestral duplications, originating from a large-scale gene duplication predating the diversification of Aphidomorpha (comprising aphids, phylloxerids, and adelgids). Genes duplicated in this ancestral wave are enriched in functions related to traits shared by Aphidomorpha, such as association with endosymbionts, and adaptation to plant defenses and phloem-sap-based diet. The ancestral nature of this duplication wave (106–227 Ma) and the lack of sufficiently conserved synteny make it difficult to conclude whether it originated from a whole-genome duplication event or, alternatively, from a burst of large-scale segmental duplications. Genome sequencing of other aphid species belonging to different Aphidomorpha and related lineages may clarify these findings.

Plasmodium vivax Malaria Viewed through the Lens of an Eradicated European Strain

Thu, 07 Nov 2019 00:00:00 GMT

Abstract
The protozoan Plasmodium vivax is responsible for 42% of all cases of malaria outside Africa. The parasite is currently largely restricted to tropical and subtropical latitudes in Asia, Oceania, and the Americas. Though, it was historically present in most of Europe before being finally eradicated during the second half of the 20th century. The lack of genomic information on the extinct European lineage has prevented a clear understanding of historical population structuring and past migrations of P. vivax. We used medical microscope slides prepared in 1944 from malaria-affected patients from the Ebro Delta in Spain, one of the last footholds of malaria in Europe, to generate a genome of a European P. vivax strain. Population genetics and phylogenetic analyses placed this strain basal to a cluster including samples from the Americas. This genome allowed us to calibrate a genomic mutation rate for P. vivax, and to estimate the mean age of the last common ancestor between European and American strains to the 15th century. This date points to an introduction of the parasite during the European colonization of the Americas. In addition, we found that some known variants for resistance to antimalarial drugs, including Chloroquine and Sulfadoxine, were already present in this European strain, predating their use. Our results shed light on the evolution of an important human pathogen and illustrate the value of antique medical collections as a resource for retrieving genomic information on pathogens from the past.

A Burst of Genetic Innovation in Drosophila Actin-Related Proteins for Testis-Specific Function

Thu, 07 Nov 2019 00:00:00 GMT

Abstract
Many cytoskeletal proteins perform fundamental biological processes and are evolutionarily ancient. For example, the superfamily of actin-related proteins (Arps) specialized early in eukaryotic evolution for diverse cellular roles in the cytoplasm and the nucleus. Despite its strict conservation across eukaryotes, we find that the Arp superfamily has undergone dramatic lineage-specific diversification in Drosophila. Our phylogenomic analyses reveal four independent Arp gene duplications that occurred in the common ancestor of the obscura group of Drosophila and have been mostly preserved in this lineage. All four obscura-specific Arp paralogs are predominantly expressed in the male germline and have evolved under positive selection. We focus our analyses on the divergent Arp2D paralog, which arose via a retroduplication event from Arp2, a component of the Arp2/3 complex that polymerizes branched actin networks. Computational modeling analyses suggest that Arp2D can replace Arp2 in the Arp2/3 complex and bind actin monomers. Together with the signature of positive selection, our findings suggest that Arp2D may augment Arp2’s functions in the male germline. Indeed, we find that Arp2D is expressed during and following male meiosis, where it localizes to distinct locations such as actin cones—specialized cytoskeletal structures that separate bundled spermatids into individual mature sperm. We hypothesize that this unprecedented burst of genetic innovation in cytoskeletal proteins may have been driven by the evolution of sperm heteromorphism in the obscura group of Drosophila.

Ancient Adaptive Lateral Gene Transfers in the Symbiotic Opalina–Blastocystis Stramenopile Lineage

Wed, 06 Nov 2019 00:00:00 GMT

Abstract
Lateral gene transfer is a very common process in bacterial and archaeal evolution, playing an important role in the adaptation to new environments. In eukaryotes, its role and frequency remain highly debated, although recent research supports that gene transfer from bacteria to diverse eukaryotes may be much more common than previously appreciated. However, most of this research focused on animals and the true phylogenetic and functional impact of bacterial genes in less-studied microbial eukaryotic groups remains largely unknown. Here, we have analyzed transcriptome data from the deep-branching stramenopile Opalinidae, common members of frog gut microbiomes, and distantly related to the well-known genus Blastocystis. Phylogenetic analyses suggest the early acquisition of several bacterial genes in a common ancestor of both lineages. Those lateral gene transfers most likely facilitated the adaptation of the free-living ancestor of the Opalinidae–Blastocystis symbiotic group to new niches in the oxygen-depleted animal gut environment.

Divergent Selection and Primary Gene Flow Shape Incipient Speciation of a Riparian Tree on Hawaii Island

Wed, 06 Nov 2019 00:00:00 GMT

Abstract
A long-standing goal of evolutionary biology is to understand the mechanisms underlying the formation of species. Of particular interest is whether or not speciation can occur in the presence of gene flow and without a period of physical isolation. Here, we investigated this process within Hawaiian Metrosideros, a hypervariable and highly dispersible woody species complex that dominates the Hawaiian Islands in continuous stands. Specifically, we investigated the origin of Metrosideros polymorpha var. newellii (newellii), a riparian ecotype endemic to Hawaii Island that is purportedly derived from the archipelago-wide M. polymorpha var. glaberrima (glaberrima). Disruptive selection across a sharp forest-riparian ecotone contributes to the isolation of these varieties and is a likely driver of newellii’s origin. We examined genome-wide variation of 42 trees from Hawaii Island and older islands. Results revealed a split between glaberrima and newellii within the past 0.3–1.2 My. Admixture was extensive between lineages within Hawaii Island and between islands, but introgression from populations on older islands (i.e., secondary gene flow) did not appear to contribute to the emergence of newellii. In contrast, recurrent gene flow (i.e., primary gene flow) between glaberrima and newellii contributed to the formation of genomic islands of elevated absolute and relative divergence. These regions were enriched for genes with regulatory functions as well as for signals of positive selection, especially in newellii, consistent with divergent selection underlying their formation. In sum, our results support riparian newellii as a rare case of incipient ecological speciation with primary gene flow in trees.

Genomic Resources for Darters (Percidae: Etheostominae) Provide Insight into Postzygotic Barriers Implicated in Speciation

Tue, 05 Nov 2019 00:00:00 GMT

Abstract
Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.

A Bayesian Framework for Inferring the Influence of Sequence Context on Point Mutations

Tue, 05 Nov 2019 00:00:00 GMT

Abstract
The probability of point mutations is expected to be highly influenced by the flanking nucleotides that surround them, known as the sequence context. This phenomenon may be mainly attributed to the enzyme that modifies or mutates the genetic material, because most enzymes tend to have specific sequence contexts that dictate their activity. Here, we develop a statistical model that allows for the detection and evaluation of the effects of different sequence contexts on mutation rates from deep population sequencing data. This task is computationally challenging, as the complexity of the model increases exponentially as the context size increases. We established our novel Bayesian method based on sparse model selection methods, with the leading assumption that the number of actual sequence contexts that directly influence mutation rates is minuscule compared with the number of possible sequence contexts. We show that our method is highly accurate on simulated data using pentanucleotide contexts, even when accounting for noisy data. We next analyze empirical population sequencing data from polioviruses and HIV-1 and detect a significant enrichment in sequence contexts associated with deamination by the cellular deaminases ADAR 1/2 and APOBEC3G, respectively. In the current era, where next-generation sequencing data are highly abundant, our approach can be used on any population sequencing data to reveal context-dependent base alterations and may assist in the discovery of novel mutable sites or editing sites.

Mitochondrial Metagenomics Reveals the Ancient Origin and Phylodiversity of Soil Mites and Provides a Phylogeny of the Acari

Thu, 31 Oct 2019 00:00:00 GMT

Abstract
High-throughput DNA methods hold great promise for phylogenetic analysis of lineages that are difficult to study with conventional molecular and morphological approaches. The mites (Acari), and in particular the highly diverse soil-dwelling lineages, are among the least known branches of the metazoan Tree-of-Life. We extracted numerous minute mites from soils in an area of mixed forest and grassland in southern Iberia. Selected specimens representing the full morphological diversity were shotgun sequenced in bulk, followed by genome assembly of short reads from the mixture, which produced >100 mitochondrial genomes representing diverse acarine lineages. Phylogenetic analyses in combination with taxonomically limited mitogenomes available publicly resulted in plausible trees defining basal relationships of the Acari. Several critical nodes were supported by ancestral-state reconstructions of mitochondrial gene rearrangements. Molecular calibration placed the minimum age for the common ancestor of the superorder Acariformes, which includes most soil-dwelling mites, to the Cambrian–Ordovician (likely within 455–552 Ma), whereas the origin of the superorder Parasitiformes was placed later in the Carboniferous-Permian. Most family-level taxa within the Acariformes were dated to the Jurassic and Triassic. The ancient origin of Acariformes and the early diversification of major extant lineages linked to the soil are consistent with a pioneering role for mites in building the earliest terrestrial ecosystems.

Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence

Fri, 25 Oct 2019 00:00:00 GMT

Abstract
Nonrecombining sex chromosomes are widely found to be more differentiated than autosomes among closely related species, due to smaller effective population size and/or to a disproportionally large-X effect in reproductive isolation. Although fungal mating-type chromosomes can also display large nonrecombining regions, their levels of differentiation compared with autosomes have been little studied. Anther-smut fungi from the Microbotryum genus are castrating pathogens of Caryophyllaceae plants with largely nonrecombining mating-type chromosomes. Using whole genome sequences of 40 fungal strains, we quantified genetic differentiation among strains isolated from the geographically overlapping North American species and subspecies of Silene virginica and S. caroliniana. We inferred that gene flow likely occurred at the early stages of divergence and then completely stopped. We identified large autosomal genomic regions with chromosomal inversions, with higher genetic divergence than the rest of the genomes and highly enriched in selective sweeps, supporting a role of rearrangements in preventing gene flow in genomic regions involved in ecological divergence. Unexpectedly, the nonrecombining mating-type chromosomes showed lower divergence than autosomes due to higher gene flow, which may be promoted by adaptive introgressions of less degenerated mating-type chromosomes. The fact that both mating-type chromosomes are always heterozygous and nonrecombining may explain such patterns that oppose to those found for XY or ZW sex chromosomes. The specific features of mating-type chromosomes may also apply to the UV sex chromosomes determining sexes at the haploid stage in algae and bryophytes and may help test general hypotheses on the evolutionary specificities of sex-related chromosomes.

OxyR Is a Convergent Target for Mutations Acquired during Adaptation to Oxidative Stress-Prone Metabolic States

Fri, 25 Oct 2019 00:00:00 GMT

Abstract
Oxidative stress is concomitant with aerobic metabolism. Thus, bacterial genomes encode elaborate mechanisms to achieve redox homeostasis. Here we report that the peroxide-sensing transcription factor, oxyR, is a common mutational target using bacterial species belonging to two genera, Escherichia coli and Vibrio natriegens, in separate growth conditions implemented during laboratory evolution. The mutations clustered in the redox active site, dimer interface, and flexible redox loop of the protein. These mutations favor the oxidized conformation of OxyR that results in constitutive expression of the genes it regulates. Independent component analysis of the transcriptome revealed that the constitutive activity of OxyR reduces DNA damage from reactive oxygen species, as inferred from the activity of the SOS response regulator LexA. This adaptation to peroxide stress came at a cost of lower growth, as revealed by calculations of proteome allocation using genome-scale models of metabolism and macromolecular expression. Further, identification of similar sequence changes in natural isolates of E. coli indicates that adaptation to oxidative stress through genetic changes in oxyR can be a common occurrence.

Asymmetric Distribution of Gene Trees Can Arise under Purifying Selection If Differences in Population Size Exist

Tue, 22 Oct 2019 00:00:00 GMT

Abstract
Incomplete lineage sorting (ILS) is an important factor that causes gene tree discordance. For gene trees of three species, under neutrality, random mating, and the absence of interspecific gene flow, ILS creates a symmetric distribution of gene trees: the gene tree that accords with the species tree has the highest frequency, and the two discordant trees are equally frequent. If the neutral condition is violated, the impact of ILS may change, altering the gene tree distribution. Here, we show that under purifying selection, even assuming that the fitness effect of mutations is constant throughout the species tree, if differences in population size exist among species, asymmetric distributions of gene trees will arise, which is different from the expectation under neutrality. In extremes, one of the discordant trees rather than the concordant tree becomes the most frequent gene tree. In addition, we found that in a real case, the position of Scandentia relative to Primate and Glires, the symmetry in the gene tree distribution can be influenced by the strength of purifying selection. In current phylogenetic inference, the impact of purifying selection on the gene tree distribution is rarely considered by researchers. This study highlights the necessity of considering this impact.

HLA Heterozygote Advantage against HIV-1 Is Driven by Quantitative and Qualitative Differences in HLA Allele-Specific Peptide Presentation

Tue, 22 Oct 2019 00:00:00 GMT

Abstract
Pathogen-mediated balancing selection is regarded as a key driver of host immunogenetic diversity. A hallmark for balancing selection in humans is the heterozygote advantage at genes of the human leukocyte antigen (HLA), resulting in improved HIV-1 control. However, the actual mechanism of the observed heterozygote advantage is still elusive. HLA heterozygotes may present a broader array of antigenic viral peptides to immune cells, possibly resulting in a more efficient cytotoxic T-cell response. Alternatively, heterozygosity may simply increase the chance to carry the most protective HLA alleles, as individual HLA alleles are known to differ substantially in their association with HIV-1 control. Here, we used data from 6,311 HIV-1-infected individuals to explore the relative contribution of quantitative and qualitative aspects of peptide presentation in HLA heterozygote advantage against HIV. Screening the entire HIV-1 proteome, we observed that heterozygous individuals exhibited a broader array of HIV-1 peptides presented by their HLA class I alleles. In addition, viral load was negatively correlated with the breadth of the HIV-1 peptide repertoire bound by an individual’s HLA variants, particularly at HLA-B. This suggests that heterozygote advantage at HLA-B is at least in part mediated by quantitative peptide presentation. We also observed higher HIV-1 sequence diversity among HLA-B heterozygous individuals, suggesting stronger evolutionary pressure from HLA heterozygosity. However, HLA heterozygotes were also more likely to carry certain HLA alleles, including the highly protective HLA-B*57:01 variant, indicating that HLA heterozygote advantage ultimately results from a combination of quantitative and qualitative effects in antigen presentation.

GBE | Most Read

Genome Biology & Evolution

Highlight—Blind as a Bat? The Genetic Basis of Echolocation in Bats and Whales

Mon, 27 Jan 2020 00:00:00 GMT

Clicks, squeaks, chirps, buzzes, etc. though they may be difficult to distinguish to our ears, such sounds are used by echolocating animals to paint a vivid picture of their surroundings. By generating a sound and then listening to how the sound waves bounce off of objects around them, these animals are able to “see” using sound. Although a number of species engage in some form of echolocation, including some birds, shrews, and even humans, the echolocation systems of bats and toothed whales (including dolphins, porpoises, killer whales, and sperm whales) are exquisitely sophisticated. Echolocation evolved independently in these animals (fig. 1) under conditions of poor visibility—the night sky for bats and deep underwater for toothed whales—enabling them to hunt for prey and navigate in complete darkness. It is a fascinating example of convergent evolution, the process by which distantly related organisms evolve similar features or adaptations. To better understand how echolocation evolved in these species, a new study in Genome Biology and Evolution, titled “Evolutionary basis of high-frequency hearing in the cochleae of echolocators revealed by comparative genomics,” takes advantage of advances in genomic analysis to investigate the origin and evolution of high-frequency hearing, an adaptation that allows echolocators to perceive ultrasonic signals.

Differential Expression in Testis and Liver Transcriptomes from Four Species of Peromyscus (Rodentia: Cricetidae)

Tue, 07 Jan 2020 00:00:00 GMT

Abstract
The genus Peromyscus represents a rapidly diverged clade of Cricetid rodents that contains multiple cryptic species and has a propensity for morphologic conservation across its members. The unresolved relationships in previously proposed phylogenies reflect a suspected rapid adaptive radiation. To identify functional groups of genes that may be important in reproductive isolation in a reoccurring fashion across the Peromyscus phylogeny, liver and testis transcriptomes from four species (P. attwateri, P. boylii, P. leucopus, and P. maniculatus) were generated and differential expression (DE) tests were conducted. Taxa were selected to represent members diverged from a common ancestor: P. attwateri + P. boylii (clade A), and P. leucopus + P. maniculatus (clade B). Comparison of clades (A vs. B) suggested that 252 transcripts had significant DE in the liver data set, whereas significant DE was identified for 657 transcripts in the testis data set. Further, 45 genes had DE isoforms in the 657 testis transcripts and most of these functioned in major reproductive roles such as acrosome assembly, spermatogenesis, and cell cycle processes (meiosis). DE transcripts in the liver mapped to more broad gene ontology terms (metabolic processes, catabolic processes, response to chemical, and regulatory processes), and DE transcripts in the testis mapped to gene ontology terms associated with reproductive processes, such as meiosis, sperm motility, acrosome assembly, and sperm–egg fusion. These results suggest that a suite of genes that conduct similar functions in the testes may be responsible for the adaptive radiation events and potential reoccurring speciation of Peromyscus in terms of reproduction through varying expression levels.

Whole Genome Sequencing and Assembly of the Asian Honey Bee Apis dorsata

Fri, 20 Dec 2019 00:00:00 GMT

Abstract
The Asian honey bee (Apis dorsata) is distinct from its more widely distributed cousin Apis mellifera by a few key characteristics. Most prominently, A. dorsata, nest in the open by forming a colony clustered around the honeycomb, whereas A. mellifera nest in concealed cavities. Additionally, the worker and reproductive castes are all of the same size in A. dorsata. In order to investigate these differences, we performed whole genome sequencing of A. dorsata using a hybrid Oxford Nanopore and Illumina approach. The 223 Mb genome has an N50 of 35 kb with the largest scaffold of 302 kb. We have found that there are many genes in the dorsata genome that are distinct from other hymenoptera and also large amounts of transposable elements, and we suggest some candidate genes for A. dorsata’s exceptional level of defensive aggression.

Comparative Plastome Analysis of Root- and Stem-Feeding Parasites of Santalales Untangle the Footprints of Feeding Mode and Lifestyle Transitions

Tue, 17 Dec 2019 00:00:00 GMT

Abstract
In plants, parasitism triggers the reductive evolution of plastid genomes (plastomes). To disentangle the molecular evolutionary associations between feeding on other plants below- or aboveground and general transitions from facultative to obligate parasitism, we analyzed 34 complete plastomes of autotrophic, root- and stem-feeding hemiparasitic, and holoparasitic Santalales. We observed inexplicable losses of housekeeping genes and tRNAs in hemiparasites and dramatic genomic reconfiguration in holoparasitic Balanophoraceae, whose plastomes have exceptionally low GC contents. Genomic changes are related primarily to the evolution of hemi- or holoparasitism, whereas the transition from a root- to a stem-feeding mode plays no major role. In contrast, the rate of molecular evolution accelerates in a stepwise manner from autotrophs to root- and then stem-feeding parasites. Already the ancestral transition to root-parasitism coincides with a relaxation of selection in plastomes. Another significant selectional shift in plastid genes occurs as stem-feeders evolve, suggesting that this derived form coincides with trophic specialization despite the retention of photosynthetic capacity. Parasitic Santalales fill a gap in our understanding of parasitism-associated plastome degeneration. We reveal that lifestyle-genome associations unfold interdependently over trophic specialization and feeding mode transitions, where holoparasitic Balanophoraceae provide a system for exploring the functional realms of plastomes.

Genome Sequences of 72 Bacterial Strains Isolated from Ectocarpus subulatus: A Resource for Algal Microbiology

Mon, 16 Dec 2019 00:00:00 GMT

Abstract
Brown algae are important primary producers and ecosystem engineers in the ocean, and Ectocarpus has been established as a laboratory model for this lineage. Like most multicellular organisms, Ectocarpus is associated with a community of microorganisms, a partnership frequently referred to as holobiont due to the tight interconnections between the components. Although genomic resources for the algal host are well established, its associated microbiome is poorly characterized from a genomic point of view, limiting the possibilities of using these types of data to study host–microbe interactions. To address this gap in knowledge, we present the annotated draft genome sequences of seventy-two cultivable Ectocarpus-associated bacteria. A screening of gene clusters related to the production of secondary metabolites revealed terpene, bacteriocin, NRPS, PKS-t3, siderophore, PKS-t1, and homoserine lactone clusters to be abundant among the sequenced genomes. These compounds may be used by the bacteria to communicate with the host and other microbes. Moreover, detoxification and provision of vitamin B pathways have been observed in most sequenced genomes, highlighting potential contributions of the bacterial metabolism toward host fitness and survival. The genomes sequenced in this study form a valuable resource for comparative genomic analyses and evolutionary surveys of alga-associated bacteria. They help establish Ectocarpus as a model for brown algal holobionts and will enable the research community to produce testable hypotheses about the molecular interactions within this complex system.

An Annotated Draft Genome of the Mountain Hare (Lepus timidus)

Fri, 13 Dec 2019 00:00:00 GMT

Abstract
Hares (genus Lepus) provide clear examples of repeated and often massive introgressive hybridization and striking local adaptations. Genomic studies on this group have so far relied on comparisons to the European rabbit (Oryctolagus cuniculus) reference genome. Here, we report the first de novo draft reference genome for a hare species, the mountain hare (Lepus timidus), and evaluate the efficacy of whole-genome re-sequencing analyses using the new reference versus using the rabbit reference genome. The genome was assembled using the ALLPATHS-LG protocol with a combination of overlapping pair and mate-pair Illumina sequencing (77x coverage). The assembly contained 32,294 scaffolds with a total length of 2.7 Gb and a scaffold N50 of 3.4 Mb. Re-scaffolding based on the rabbit reference reduced the total number of scaffolds to 4,205 with a scaffold N50 of 194 Mb. A correspondence was found between 22 of these hare scaffolds and the rabbit chromosomes, based on gene content and direct alignment. We annotated 24,578 protein coding genes by combining ab-initio predictions, homology search, and transcriptome data, of which 683 were solely derived from hare-specific transcriptome data. The hare reference genome is therefore a new resource to discover and investigate hare-specific variation. Similar estimates of heterozygosity and inferred demographic history profiles were obtained when mapping hare whole-genome re-sequencing data to the new hare draft genome or to alternative references based on the rabbit genome. Our results validate previous reference-based strategies and suggest that the chromosome-scale hare draft genome should enable chromosome-wide analyses and genome scans on hares.

Emergence and Evolution of ERM Proteins and Merlin in Metazoans

Thu, 12 Dec 2019 00:00:00 GMT

Abstract
Ezrin, radixin, moesin, and merlin are cytoskeletal proteins, whose functions are specific to metazoans. They participate in cell cortex rearrangement, including cell–cell contact formation, and play an important role in cancer progression. Here, we have performed a comprehensive phylogenetic analysis of the proteins spanning 87 species. The results describe a possible mechanism for the protein family origin in the root of Metazoa, paralogs diversification in vertebrates, and acquisition of novel functions, including tumor suppression. In addition, a merlin paralog, present in most vertebrates but lost in mammals, has been described here for the first time. We have also highlighted a set of amino acid variations within the conserved motifs as the candidates for determining physiological differences between ERM paralogs.

Microsporidia with Vertical Transmission Were Likely Shaped by Nonadaptive Processes

Wed, 11 Dec 2019 00:00:00 GMT

Abstract
Microsporidia have the leanest genomes among eukaryotes, and their physiological and genomic simplicity has been attributed to their intracellular, obligate parasitic life-style. However, not all microsporidia genomes are small or lean, with the largest dwarfing the smallest ones by at least an order of magnitude. To better understand the evolutionary mechanisms behind this genomic diversification, we explore here two clades of microsporidia with distinct life histories, Ordospora and Hamiltosporidium, parasitizing the same host species, Daphnia magna. Based on seven newly assembled genomes, we show that mixed-mode transmission (the combination of horizontal and vertical transmission), which occurs in Hamiltosporidium, is found to be associated with larger and AT-biased genomes, more genes, and longer intergenic regions, as compared with the exclusively horizontally transmitted Ordospora. Furthermore, the Hamiltosporidium genome assemblies contain a variety of repetitive elements and long segmental duplications. We show that there is an excess of nonsynonymous substitutions in the microsporidia with mixed-mode transmission, which cannot be solely attributed to the lack of recombination, suggesting that bursts of genome size in these microsporidia result primarily from genetic drift. Overall, these findings suggest that the switch from a horizontal-only to a mixed mode of transmission likely produces population bottlenecks in Hamiltosporidium species, therefore reducing the effectiveness of natural selection, and allowing their genomic features to be largely shaped by nonadaptive processes.

A High-Quality Reference Genome Assembly of the Saltwater Crocodile, Crocodylus porosus, Reveals Patterns of Selection in Crocodylidae

Tue, 10 Dec 2019 00:00:00 GMT

Abstract
Crocodilians are an economically, culturally, and biologically important group. To improve researchers’ ability to study genome structure, evolution, and gene regulation in the clade, we generated a high-quality de novo genome assembly of the saltwater crocodile, Crocodylus porosus, from Illumina short read data from genomic libraries and in vitro proximity-ligation libraries. The assembled genome is 2,123.5 Mb, with N50 scaffold size of 17.7 Mb and N90 scaffold size of 3.8 Mb. We then annotated this new assembly, increasing the number of annotated genes by 74%. In total, 96% of 23,242 annotated genes were associated with a functional protein domain. Furthermore, multiple noncoding functional regions and mappable genetic markers were identified. Upon analysis and overlapping the results of branch length estimation and site selection tests for detecting potential selection, we found 16 putative genes under positive selection in crocodilians, 10 in C. porosus and 6 in Alligator mississippiensis. The annotated C. porosus genome will serve as an important platform for osmoregulatory, physiological, and sex determination studies, as well as an important reference in investigating the phylogenetic relationships of crocodilians, birds, and other tetrapods.

Evolutionary History of the Toll-Like Receptor Gene Family across Vertebrates

Wed, 04 Dec 2019 00:00:00 GMT

Abstract
Adaptation to a wide range of pathogenic environments is a major aspect of the ecological adaptations of vertebrates during evolution. Toll-like receptors (TLRs) are ancient membrane-bound sensors in animals and are best known for their roles in detecting and defense against invading pathogenic microorganisms. To understand the evolutionary history of the vertebrate TLR gene family, we first traced the origin of single-cysteine cluster TLRs that share the same protein architecture with vertebrate TLRs in early-branching animals and then analyzed all members of the TLR family in over 200 species covering all major vertebrate clades. Our results indicate that although the emergence of single-cysteine cluster TLRs predates the separation of bilaterians and cnidarians, most vertebrate TLR members originated shortly after vertebrate emergence. Phylogenetic analyses divided 1,726 vertebrate TLRs into 8 subfamilies, and TLR3 may represent the most ancient subfamily that emerged before the branching of deuterostomes. Our analysis reveals that purifying selection predominated in the evolution of all vertebrate TLRs, with mean dN/dS (ω) values ranging from 0.082 for TLR21 in birds to 0.434 for TLR11 in mammals. However, we did observe patterns of positive selection acting on specific codons (527 of 60,294 codons across all vertebrate TLRs, 8.7‰), which are significantly concentrated in ligand-binding extracellular domains and suggest host–pathogen coevolutionary interactions. Additionally, we found stronger positive selection acting on nonviral compared with viral TLRs, indicating the more essential nonredundant function of viral TLRs in host immunity. Taken together, our findings provide comprehensive insight into the complex evolutionary processes of the vertebrate TLR gene family, involving gene duplication, pseudogenization, purification, and positive selection.

The Genome of the Blind Soil-Dwelling and Ancestrally Wingless Dipluran Campodea augens: A Key Reference Hexapod for Studying the Emergence of Insect Innovations

Tue, 03 Dec 2019 00:00:00 GMT

Abstract
The dipluran two-pronged bristletail Campodea augens is a blind ancestrally wingless hexapod with the remarkable capacity to regenerate lost body appendages such as its long antennae. As sister group to Insecta (sensu stricto), Diplura are key to understanding the early evolution of hexapods and the origin and evolution of insects. Here we report the 1.2-Gb draft genome of C. augens and results from comparative genomic analyses with other arthropods. In C. augens, we uncovered the largest chemosensory gene repertoire of ionotropic receptors in the animal kingdom, a massive expansion that might compensate for the loss of vision. We found a paucity of photoreceptor genes mirroring at the genomic level the secondary loss of an ancestral external photoreceptor organ. Expansions of detoxification and carbohydrate metabolism gene families might reflect adaptations for foraging behavior, and duplicated apoptotic genes might underlie its high regenerative potential. The C. augens genome represents one of the key references for studying the emergence of genomic innovations in insects, the most diverse animal group, and opens up novel opportunities to study the under-explored biology of diplurans.

The Mitogenome of Norway Spruce and a Reappraisal of Mitochondrial Recombination in Plants

Wed, 27 Nov 2019 00:00:00 GMT

Abstract
Plant mitogenomes can be difficult to assemble because they are structurally dynamic and prone to intergenomic DNA transfers, leading to the unusual situation where an organelle genome is far outnumbered by its nuclear counterparts. As a result, comparative mitogenome studies are in their infancy and some key aspects of genome evolution are still known mainly from pregenomic, qualitative methods. To help address these limitations, we combined machine learning and in silico enrichment of mitochondrial-like long reads to assemble the bacterial-sized mitogenome of Norway spruce (Pinaceae: Picea abies). We conducted comparative analyses of repeat abundance, intergenomic transfers, substitution and rearrangement rates, and estimated repeat-by-repeat homologous recombination rates. Prompted by our discovery of highly recombinogenic small repeats in P. abies, we assessed the genomic support for the prevailing hypothesis that intramolecular recombination is predominantly driven by repeat length, with larger repeats facilitating DNA exchange more readily. Overall, we found mixed support for this view: Recombination dynamics were heterogeneous across vascular plants and highly active small repeats (ca. 200 bp) were present in about one-third of studied mitogenomes. As in previous studies, we did not observe any robust relationships among commonly studied genome attributes, but we identify variation in recombination rates as a underinvestigated source of plant mitogenome diversity.

Genome Assembly of the Dogface Butterfly Zerene cesonia

Fri, 22 Nov 2019 00:00:00 GMT

Abstract
Comparisons of high-quality, reference butterfly, and moth genomes have been instrumental to advancing our understanding of how hybridization, and natural selection drive genomic change during the origin of new species and novel traits. Here, we present a genome assembly of the Southern Dogface butterfly, Zerene cesonia (Pieridae) whose brilliant wing colorations have been implicated in developmental plasticity, hybridization, sexual selection, and speciation. We assembled 266,407,278 bp of the Z. cesonia genome, which accounts for 98.3% of the estimated 271 Mb genome size. Using a hybrid approach involving Chicago libraries with Hi-Rise assembly and a diploid Meraculous assembly, the final haploid genome was assembled. In the final assembly, nearly all autosomes and the Z chromosome were assembled into single scaffolds. The largest 29 scaffolds accounted for 91.4% of the genome assembly, with the remaining ∼8% distributed among another 247 scaffolds and overall N50 of 9.2 Mb. Tissue-specific RNA-seq informed annotations identified 16,442 protein-coding genes, which included 93.2% of the arthropod Benchmarking Universal Single-Copy Orthologs (BUSCO). The Z. cesonia genome assembly had ∼9% identified as repetitive elements, with a transposable element landscape rich in helitrons. Similar to other Lepidoptera genomes, Z. cesonia showed a high conservation of chromosomal synteny. The Z. cesonia assembly provides a high-quality reference for studies of chromosomal arrangements in the Pierid family, as well as for population, phylo, and functional genomic studies of adaptation and speciation.

Evolutionary Basis of High-Frequency Hearing in the Cochleae of Echolocators Revealed by Comparative Genomics

Fri, 15 Nov 2019 00:00:00 GMT

Abstract
High-frequency hearing is important for the survival of both echolocating bats and whales, but our understanding of its genetic basis is scattered and segmented. In this study, we combined RNA-Seq and comparative genomic analyses to obtain insights into the comprehensive gene expression profile of the cochlea and the adaptive evolution of hearing-related genes. A total of 144 genes were found to have been under positive selection in various species of echolocating bats and toothed whales, 34 of which were identified to be related to hearing behavior or auditory processes. Subsequently, multiple physiological processes associated with those genes were found to have adaptively evolved in echolocating bats and toothed whales, including cochlear bony development, antioxidant activity, ion balance, and homeostatic processes, along with signal transduction. In addition, abundant convergent/parallel genes and sites were detected between different pairs of echolocator species; however, no specific hearing-related physiological pathways were enriched by them and almost all of the convergent/parallel signals were selectively neutral, as previously reported. Notably, two adaptive parallel evolved sites in TECPR2 were shown to have been under positive selection, indicating their functional importance for the evolution of echolocation and high-frequency hearing in laryngeal echolocating bats. This study deepens our understanding of the genetic bases underlying high-frequency hearing in the cochlea of echolocating bats and toothed whales.

Comparative Genomic Analysis of the Pheromone Receptor Class 1 Family (V1R) Reveals Extreme Complexity in Mouse Lemurs (Genus, Microcebus) and a Chromosomal Hotspot across Mammals

Thu, 14 Nov 2019 00:00:00 GMT

Abstract
Sensory gene families are of special interest for both what they can tell us about molecular evolution and what they imply as mediators of social communication. The vomeronasal type-1 receptors (V1Rs) have often been hypothesized as playing a fundamental role in driving or maintaining species boundaries given their likely function as mediators of intraspecific mate choice, particularly in nocturnal mammals. Here, we employ a comparative genomic approach for revealing patterns of V1R evolution within primates, with a special focus on the small-bodied nocturnal mouse and dwarf lemurs of Madagascar (genera Microcebus and Cheirogaleus, respectively). By doubling the existing genomic resources for strepsirrhine primates (i.e. the lemurs and lorises), we find that the highly speciose and morphologically cryptic mouse lemurs have experienced an elaborate proliferation of V1Rs that we argue is functionally related to their capacity for rapid lineage diversification. Contrary to a previous study that found equivalent degrees of V1R diversity in diurnal and nocturnal lemurs, our study finds a strong correlation between nocturnality and V1R elaboration, with nocturnal lemurs showing elaborate V1R repertoires and diurnal lemurs showing less diverse repertoires. Recognized subfamilies among V1Rs show unique signatures of diversifying positive selection, as might be expected if they have each evolved to respond to specific stimuli. Furthermore, a detailed syntenic comparison of mouse lemurs with mouse (genus Mus) and other mammalian outgroups shows that orthologous mammalian subfamilies, predicted to be of ancient origin, tend to cluster in a densely populated region across syntenic chromosomes that we refer to as a V1R “hotspot.”

The Mitochondrial Genome of Eleusine indica and Characterization of Gene Content within Poaceae

Wed, 23 Oct 2019 00:00:00 GMT

Abstract
Plant mitochondrial (mt) genome assembly provides baseline data on size, structure, and gene content, but resolving the sequence of these large and complex organelle genomes remains challenging due to fragmentation, frequent recombination, and transfers of DNA from neighboring plastids. The mt genome for Eleusine indica (Poaceae: goosegrass) is comprehensibly analyzed here, providing key reference data for an economically significant invasive species that is also the maternal parent of the allotetraploid crop Finger millet (Eleusine coracana). The assembled E. indica genome contains 33 protein coding genes, 6 rRNA subunits, 24 tRNA, 8 large repetitive regions 15 kb of transposable elements across a total of 520,691 bp. Evidence of RNA editing and loss of rpl2, rpl5, rps14, rps11, sdh4, and sdh3 genes is evaluated in the context of an updated survey of mt genomic gene content across the grasses through an analysis of publicly available data. Hypothesized patterns of Poaceae mt gene loss are examined in a phylogenetic context to clarify timing, showing that rpl2 was transferred to the nucleus from the mitochondrion prior to the origin of the PACMAD clade.

Impact of Mutation Rate and Selection at Linked Sites on DNA Variation across the Genomes of Humans and Other Homininae

Wed, 09 Oct 2019 00:00:00 GMT

Abstract
DNA diversity varies across the genome of many species. Variation in diversity across a genome might arise from regional variation in the mutation rate, variation in the intensity and mode of natural selection, and regional variation in the recombination rate. We show that both noncoding and nonsynonymous diversity are positively correlated to a measure of the mutation rate and the recombination rate and negatively correlated to the density of conserved sequences in 50 kb windows across the genomes of humans and nonhuman homininae. Interestingly, we find that although noncoding diversity is equally affected by these three genomic variables, nonsynonymous diversity is mostly dominated by the density of conserved sequences. The positive correlation between diversity and our measure of the mutation rate seems to be largely a direct consequence of regions with higher mutation rates having more diversity. However, the positive correlation with recombination rate and the negative correlation with the density of conserved sequences suggest that selection at linked sites also affect levels of diversity. This is supported by the observation that the ratio of the number of nonsynonymous to noncoding polymorphisms is negatively correlated to a measure of the effective population size across the genome. We show these patterns persist even when we restrict our analysis to GC-conservative mutations, demonstrating that the patterns are not driven by GC biased gene conversion. In conclusion, our comparative analyses describe how recombination rate, gene density, and mutation rate interact to produce the patterns of DNA diversity that we observe along the hominine genomes.

Transcriptome-Wide Patterns of the Genetic and Expression Variations in Two Sympatric Schizothoracine Fishes in a Tibetan Plateau Glacier Lake

Wed, 09 Jan 2019 00:00:00 GMT

Abstract
Sympatric speciation remains a central focus of evolutionary biology. Although some evidence shows speciation occurring in this way, little is known about the gene expression evolution and the characteristics of population genetics as species diverge. Two closely related Gymnocypris fish (Gymnocypris chui and Gymnocypris scleracanthus), which come from a small glacier lake in the Tibetan Plateau, Lake Langcuo, exist a possible incipient sympatric adaptive ecological speciation. We generated large amounts of RNA-Seq data from multiple individuals and tissues from each of the two species and compared gene expression patterns and genetic polymorphisms between them. Ordination analysis separated samples by organ rather than by species. The degree of expression difference between organs within and between species was different. Phylogenetic analyses indicated that the two closely related taxa formed a monophyletic complex. Population structure analysis displayed two distinctly divergent clusters of G. chui and G. scleracanthus populations. By contrast, G. scleracanthus population genetic diversity is higher than that of G. chui. Considerable sites of the two populations were differentiated with a coefficient of FST = 0.25–0.50, implying that a small proportion of loci nevertheless exhibited deep divergence in two comparisons. Concomitantly, putatively selected genes during speciation revealed functional categories are enriched in bone morphogenesis, cell growth, neurogenetics, enzyme activity, and binding activity in G. chui population. In contrast, nutrition and localization were highlighted in G. scleracanthus. Collectively, morphological traits and dietary preference combine with genetic variation and expression variation, probably contributed to the incipient speciation of two sympatric populations.