Just How Blind Are Bats? Color Vision Gene Study Examines Key Sensory Tradeoffs

Mon, 21 Jan 2019 00:00:00 GMT

Could bats’ cave-dwelling nocturnal habits over eons enhanced their echolocation acoustic abilities, but also spurred their loss of vision?

Society for Molecular Biology and Evolution, Council and Business Meetings, 2018, Yokohama, Japan

Fri, 18 Jan 2019 00:00:00 GMT

Treasurer’s Report for Financial Year (FY) 2017Prepared by Jeffrey L. Thorne, SMBE Treasurer (2018–present) and Juliette de Meaux, SMBE Treasurer (2015–2017)

Fri, 18 Jan 2019 00:00:00 GMT

Society’s Net Assets as of May 31, 2018:

MBE Citation Classics (2019 Edition)

Wed, 09 Jan 2019 00:00:00 GMT

Molecular Biology and Evolution (MBE) is pleased to release a list of “Citation Classics” to celebrate and highlight the diversity and impact of MBE publications in molecular evolutionary research. “Early” (1983–2013) and “Recent” (2014–2018) Citation Classics are selected separately. To emphasize the durability of our early classics, we choose articles published between 1983 and 2013 that have been highly cited within the past 5 years (2013–2017). Yearly citation counts of articles published between 1983 and 2013 were obtained from Thomson Reuters Web of Science on November 19, 2018. From the resulting set, we identified 20 publications reporting biological discoveries and 20 publications reporting methods or resources that maintained the highest citation counts from 2014 to 2018. We have designated these articles as “Golden Classics.” For the “Recent” category of Citation Classics, ten discovery and ten method/resource publications were selected based on their citations accrued per fractional years since print publication. Articles in both categories are listed from most recent to oldest publication date. Overall, <1% of articles are designated as MBE Citation Classics.

A Report by the Editor-in-Chief for Molecular Biology and Evolution (MBE), Volume 34

Fri, 14 Dec 2018 00:00:00 GMT

Molecular Biology and Evolution is a prominent and highly respected society-owned journal within an increasingly competitive scientific publication landscape. MBE is owned exclusively by the Society for Molecular Biology and Evolution and is published by the Oxford University Press. Society ownership ensures that MBE is created by and for the society members, and that the proceeds from the journal publication benefit the scientific community through the sponsorship of annual and satellite meetings and through travel and research support for young and established scientists. MBE continues to be published monthly both in print and online editions, and provides subscribers worldwide with access to top-quality research at the intersection of molecular biology and evolution.

As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats

Fri, 23 Nov 2018 00:00:00 GMT

Through their unique use of sophisticated laryngeal echolocation bats are considered sensory specialists amongst mammals and represent an excellent model in which to explore sensory perception. Although several studies have shown that the evolution of vision is linked to ecological niche adaptation in other mammalian lineages, this has not yet been fully explored in bats. Recent molecular analysis of the opsin genes, which encode the photosensitive pigments underpinning color vision, have implicated high-duty cycle (HDC) echolocation and the adoption of cave roosting habits in the degeneration of color vision in bats. However, insufficient sampling of relevant taxa has hindered definitive testing of these hypotheses. To address this, novel sequence data was generated for the SWS1 and MWS/LWS opsin genes and combined with existing data to comprehensively sample species representing diverse echolocation types and niches (SWS1 n = 115; MWS/LWS n = 45). A combination of phylogenetic analysis, ancestral state reconstruction, and selective pressure analyses were used to reconstruct the evolution of these visual pigments in bats and revealed that although both genes are evolving under purifying selection in bats, MWS/LWS is highly conserved but SWS1 is highly variable. Spectral tuning analyses revealed that MWS/LWS opsin is tuned to a long wavelength, 555–560 nm in the bat ancestor and the majority of extant taxa. The presence of UV vision in bats is supported by our spectral tuning analysis, but phylogenetic analyses demonstrated that the SWS1 opsin gene has undergone pseudogenization in several lineages. We do not find support for a link between the evolution of HDC echolocation and the pseudogenization of the SWS1 gene in bats, instead we show the SWS1 opsin is functional in the HDC echolocator, Pteronotus parnellii. Pseudogenization of the SWS1 is correlated with cave roosting habits in the majority of pteropodid species. Together these results demonstrate that the loss of UV vision in bats is more widespread than was previously considered and further elucidate the role of ecological niche specialization in the evolution of vision in bats.

Genome-Wide Regulatory Adaptation Shapes Population-Level Genomic Landscapes in Heliconius

Mon, 19 Nov 2018 00:00:00 GMT

Cis-regulatory evolution is an important engine of organismal diversification. Although recent studies have looked at genomic patterns of regulatory evolution between species, we still have a poor understanding of the magnitude and nature of regulatory variation within species. Here, we examine the evolution of regulatory element activity over wing development in three Heliconius erato butterfly populations to determine how regulatory variation is associated with population structure. We show that intraspecific divergence in chromatin accessibility and regulatory activity is abundant, and that regulatory variants are spatially clustered in the genome. Regions with strong population structure are highly enriched for regulatory variants, and enrichment patterns are associated with developmental stage and gene expression. We also found that variable regulatory elements are particularly enriched in species-specific genomic regions and long interspersed nuclear elements. Our findings suggest that genome-wide selection on chromatin accessibility and regulatory activity is an important force driving patterns of genomic divergence within Heliconius species. This work also provides a resource for the study of gene regulatory evolution in H. erato and other heliconiine butterflies.

Loss of Gene Body Methylation in Eutrema salsugineum Is Associated with Reduced Gene Expression

Tue, 06 Nov 2018 00:00:00 GMT

Gene body methylation (gbM) is typically characterized by DNA methylation in the CG context within coding regions and is associated with constitutive genes that have moderate to high expression levels. A recent study discovered the loss of gbM in two plant species (Eutrema salsugineum and Conringia planisiliqua), illustrating that gbM is not necessary for survival and reproduction. The same paper stated there was no detectable effect of gbM loss on gene expression (GE). Here, we reanalyzed the GE data and accounted for experimental variability in expression level estimates. We show that the loss of gbM in E. salsugineum is associated with a small but highly significant decrease in GE relative to the closely related species Arabidospis thaliana. Our results are consistent with various evolutionary analyses that suggest gbM has a function, perhaps as a homeostatic effect on GE.

Recombination and Large Structural Variations Shape Interspecific Edible Bananas Genomes

Tue, 06 Nov 2018 00:00:00 GMT

Admixture and polyploidization are major recognized eukaryotic genome evolutionary processes. Their impacts on genome dynamics vary among systems and are still partially deciphered. Many banana cultivars are triploid (sometimes diploid) interspecific hybrids between Musa acuminata (A genome) and M. balbisiana (B genome). They have no or very low fertility, are vegetatively propagated and have been classified as “AB,” “AAB,” or “ABB” based on morphological characters. We used NGS sequence data to characterize the A versus B chromosome composition of nine diploid and triploid interspecific cultivars, to compare the chromosome structures of A and B genomes and analyze A/B chromosome segregations in a polyploid context. We showed that interspecific recombination occurred frequently between A and B chromosomes. We identified two large structural variations between A and B genomes, a reciprocal translocation and an inversion that locally affected recombination and led to segregation distortion and aneuploidy in a triploid progeny. Interspecific recombination and large structural variations explained the mosaic genomes observed in edible bananas. The unprecedented resolution in deciphering their genome structure allowed us to start revisiting the origins of banana cultivars and provided new information to gain insight into the impact of interspecificity on genome evolution. It will also facilitate much more effective assessment of breeding strategies.

On the Regulatory Evolution of New Genes Throughout Their Life History

Sat, 03 Nov 2018 00:00:00 GMT

Every gene has a birthplace and an age, that is, a cis-regulatory environment and an evolution lifespan since its origination, yet how the two shape the evolution trajectories of genes remains unclear. Here, we address this basic question by comparing phylogenetically dated new genes in the context of both their ages and origination mechanisms. In both Drosophila and vertebrates, we confirm a clear “out of the testis” transition from the specifically expressed young genes to the broadly expressed old housekeeping genes, observed only in testis but not in other tissues. Many new genes have gained important functions during embryogenesis, manifested as either specific activation at maternal–zygotic transition, or different spatiotemporal expressions from their parental genes. These expression patterns are largely driven by an age-dependent evolution of cis-regulatory environment. We discover that retrogenes are more frequently born in a pre-existing repressive regulatory domain, and are more diverged in their enhancer repertoire than the DNA-based gene duplications. During evolution, new gene duplications gradually gain active histone modifications and undergo more enhancer turnovers when becoming older, but exhibit complex trends of gaining or losing repressive histone modifications in Drosophila or vertebrates, respectively. Interestingly, vertebrate new genes exhibit an “into the testis” epigenetic transition that older genes become more likely to be co-occupied by both active and repressive (“bivalent”) histone modifications specifically in testis. Our results uncover the regulatory mechanisms underpinning the stepwise acquisition of novel and complex functions by new genes, and illuminate the general evolution trajectory of genes throughout their life history.

A Polygenic Genetic Architecture of Flowering Time in the Worldwide Arabidopsis thaliana Population

Fri, 02 Nov 2018 00:00:00 GMT

Here, we report an empirical study of the polygenic basis underlying the evolution of complex traits. Flowering time variation measured at 10 and 16°C in the 1,001-genomes Arabidopsis thaliana collection of natural accessions were used as a model. The polygenic architecture of flowering time was defined as the 48 loci that were significantly associated with flowering time—at 10 and/or 16°C and/or their difference—in this population. Contributions from alleles at flowering time associated loci to global and local adaptation were explored by evaluating their distribution across genetically and geographically defined subpopulations across the native range of the species. The dynamics in the genetic architecture of flowering time in response to temperature was evaluated by estimating how the effects of these loci on flowering changed with growth temperature. Overall, the genetic basis of flowering time was stable—about 2/3 of the flowering time loci had similar effects at 10°C and 16°C—but many loci were involved in gene by temperature interactions. Globally present alleles, mostly of moderate effect, contributed to the differences in flowering times between the subpopulations via subtle changes in allele frequencies. More extreme local adaptations were, on several occasions, due to regional alleles with relatively large effects, and their linkage disequilibrium-patterns suggest coevolution of functionally connected alleles within local populations. Overall, these findings provide a significant contribution to our understanding about the possible modes of global and local evolution of a complex adaptive trait in A. thaliana.

Detection of Shared Balancing Selection in the Absence of Trans-Species Polymorphism

Wed, 31 Oct 2018 00:00:00 GMT

Trans-species polymorphism has been widely used as a key sign of long-term balancing selection across multiple species. However, such sites are often rare in the genome and could result from mutational processes or technical artifacts. Few methods are yet available to specifically detect footprints of trans-species balancing selection without using trans-species polymorphic sites. In this study, we develop summary- and model-based approaches that are each specifically tailored to uncover regions of long-term balancing selection shared by a set of species by using genomic patterns of intraspecific polymorphism and interspecific fixed differences. We demonstrate that our trans-species statistics have substantially higher power than single-species approaches to detect footprints of trans-species balancing selection, and are robust to those that do not affect all tested species. We further apply our model-based methods to human and chimpanzee whole-genome sequencing data. In addition to the previously established major histocompatibility complex and malaria resistance-associated FREM3/GYPE regions, we also find outstanding genomic regions involved in barrier integrity and innate immunity, such as the GRIK1/CLDN17 intergenic region, and the SLC35F1 and ABCA13 genes. Our findings not only echo the significance of pathogen defense but also reveal novel candidates in maintaining balanced polymorphisms across human and chimpanzee lineages. Finally, we show that these trans-species statistics can be applied to and work well for an arbitrary number of species, and integrate them into open-source software packages for ease of use by the scientific community.

Changes in Biological Pathways During 6,000 Years of Civilization in Europe

Tue, 30 Oct 2018 00:00:00 GMT

The beginning of civilization was a turning point in human evolution. With increasing separation from the natural environment, mankind stimulated new adaptive reactions in response to new environmental factors. In this paper, we describe direct signs of these reactions in the European population during the past 6,000 years. By comparing whole-genome data between Late Neolithic/Bronze Age individuals and modern Europeans, we revealed biological pathways that are significantly differently enriched in nonsynonymous single nucleotide polymorphisms in these two groups and which therefore could be shaped by cultural practices during the past six millennia. They include metabolic transformations, immune response, signal transduction, physical activity, sensory perception, reproduction, and cognitive functions. We demonstrated that these processes were influenced by different types of natural selection. We believe that our study opens new perspectives for more detailed investigations about when and how civilization has been modifying human genomes.

Evolution of Portulacineae Marked by Gene Tree Conflict and Gene Family Expansion Associated with Adaptation to Harsh Environments

Mon, 29 Oct 2018 00:00:00 GMT

Several plant lineages have evolved adaptations that allow survival in extreme and harsh environments including many families within the plant clade Portulacineae (Caryophyllales) such as the Cactaceae, Didiereaceae, and Montiaceae. Here, using newly generated transcriptomic data, we reconstructed the phylogeny of Portulacineae and examined potential correlates between molecular evolution and adaptation to harsh environments. Our phylogenetic results were largely congruent with previous analyses, but we identified several early diverging nodes characterized by extensive gene tree conflict. For particularly contentious nodes, we present detailed information about the phylogenetic signal for alternative relationships. We also analyzed the frequency of gene duplications, confirmed previously identified whole genome duplications (WGD), and proposed a previously unidentified WGD event within the Didiereaceae. We found that the WGD events were typically associated with shifts in climatic niche but did not find a direct association with WGDs and diversification rate shifts. Diversification shifts occurred within the Portulacaceae, Cactaceae, and Anacampserotaceae, and whereas these did not experience WGDs, the Cactaceae experienced extensive gene duplications. We examined gene family expansion and molecular evolutionary patterns with a focus on genes associated with environmental stress responses and found evidence for significant gene family expansion in genes with stress adaptation and clades found in extreme environments. These results provide important directions for further and deeper examination of the potential links between molecular evolutionary patterns and adaptation to harsh environments.

Phylotranscriptomic Insights into the Diversification of Endothermic Thunnus Tunas

Fri, 26 Oct 2018 00:00:00 GMT

Birds, mammals, and certain fishes, including tunas, opahs and lamnid sharks, are endothermic, conserving internally generated, metabolic heat to maintain body or tissue temperatures above that of the environment. Bluefin tunas are commercially important fishes worldwide, and some populations are threatened. They are renowned for their endothermy, maintaining elevated temperatures of the oxidative locomotor muscle, viscera, brain and eyes, and occupying cold, productive high-latitude waters. Less cold-tolerant tunas, such as yellowfin tuna, by contrast, remain in warm-temperate to tropical waters year-round, reproducing more rapidly than most temperate bluefin tuna populations, providing resiliency in the face of large-scale industrial fisheries. Despite the importance of these traits to not only fisheries but also habitat utilization and responses to climate change, little is known of the genetic processes underlying the diversification of tunas. In collecting and analyzing sequence data across 29,556 genes, we found that parallel selection on standing genetic variation is associated with the evolution of endothermy in bluefin tunas. This includes two shared substitutions in genes encoding glycerol-3 phosphate dehydrogenase, an enzyme that contributes to thermogenesis in bumblebees and mammals, as well as four genes involved in the Krebs cycle, oxidative phosphorylation, β-oxidation, and superoxide removal. Using phylogenetic techniques, we further illustrate that the eight Thunnus species are genetically distinct, but found evidence of mitochondrial genome introgression across two species. Phylogeny-based metrics highlight conservation needs for some of these species.

Extreme Lewontin’s Paradox in Ubiquitous Marine Phytoplankton Species

Tue, 23 Oct 2018 00:00:00 GMT

Larger populations are expected to have larger genetic diversity. However, as pointed out by Lewontin in 1974, the range of population sizes exceeds the range of genetic diversity by many orders of magnitude (a.k.a. “Lewontin’s paradox,” LP). The reasons for LP remain obscure. Here, This paper reports an extreme case of LP in astronomically large populations of the ubiquitous unicellular marine phytoplankton species Emiliania huxleyi (Haptophyta)—the species that accounts for 10–20% of primary productivity in the oceans and its blooms are so extensive that they are visible from space. This study demonstrates that despite the wide distribution and enormous population size, the world-wide sample of E. huxleyi strains with sequenced genomes represents a single cohesive species and contains surprisingly limited genetic diversity (π ∼ 0.006 per silent site). The patterns of polymorphism reveal even larger populations in the past, and frequent recombination (ρ ∼ 0.006) throughout the genome, ruling out demographic history and asexual reproduction as possible causes of low polymorphism in E. huxleyi. Natural selection wiping out genetic diversity at linked sites (a.k.a. “genetic draft”) must be strong and frequent to account for low polymorphism in E. huxleyi. This study sheds the first light on poorly understood evolutionary genetic processes in astronomically large populations of marine microplankton.

Tanglegrams Are Misleading for Visual Evaluation of Tree Congruence

Tue, 23 Oct 2018 00:00:00 GMT

Evolutionary Biologists are often faced with the need to compare phylogenetic trees. One popular method consists in visualizing the trees face to face with links connecting matching taxa. These tanglegrams are optimized beforehand so that the number of lines crossing (the entanglement) is minimal. This representation is implicitly justified by the expectation that the level of entanglement is correlated with the level of similarity (or congruence) between the trees compared. Using simulations, I show that this correlation is actually very weak, which should preclude the use of such technique for getting insight into the level of congruence between trees.

Functional Consequences of the Evolution of Matrimony, a Meiosis-Specific Inhibitor of Polo Kinase

Tue, 23 Oct 2018 00:00:00 GMT

Meiosis is a defining characteristic of eukaryotes, believed to have evolved only once, over one billion years ago. While the general progression of meiotic events is conserved across multiple diverse organisms, the specific pathways and proteins involved can be highly divergent, even within species from the same genus. Here we investigate the rapid evolution of Matrimony (Mtrm), a female meiosis-specific regulator of Polo kinase (Polo) in Drosophila. Mtrm physically interacts with Polo and is required to restrict the activity of Polo during meiosis. Despite Mtrm’s critical role in meiosis, sequence conservation within the genus Drosophila is poor. To explore the functional significance of this rapid divergence, we expressed Mtrm proteins from 12 different Drosophila species in the Drosophila melanogaster female germline. Distantly related Mtrm homologs are able to both physically interact with D. melanogaster Polo and rescue the meiotic defects seen in mtrm mutants. However, these distant homologs are not properly degraded after the completion of meiosis. Rather, they continue to inhibit Polo function in the early embryo, resulting in dominant maternal-effect lethality. We show that the ability of Mtrm to be properly degraded, and thus release Polo, is partially due to residues or motifs found within Mtrm’s least-conserved regions. We hypothesize that, while Mtrm regions critical for its meiotic function are under strong purifying selection, changes that occurred in its unconserved regions may have been advantageous, potentially by affecting the timing or duration of meiosis and/or the early embryonic divisions.

Functional Conservation of a Developmental Switch in Mammals since the Jurassic Age

Mon, 08 Oct 2018 00:00:00 GMT

ThPOK is a “master regulator” of T lymphocyte lineage choice, whose presence or absence is sufficient to dictate development to the CD4 or CD8 lineages, respectively. Induction of ThPOK is transcriptionally regulated, via a lineage-specific silencer element, Sil^ThPOK. Here, we take advantage of the available genome sequence data as well as site-specific gene targeting technology, to evaluate the functional conservation of ThPOK regulation across mammalian evolution, and assess the importance of motif grammar (order and orientation of TF binding sites) on Sil^ThPOK function in vivo. We make three important points: First, the Sil^ThPOK is present in marsupial and placental mammals, but is not found in available genome assemblies of nonmammalian vertebrates, indicating that it arose after divergence of mammals from other vertebrates. Secondly, by replacing the murine Sil^ThPOK in situ with its marsupial equivalent using a knockin approach, we demonstrate that the marsupial Sil^ThPOK supports correct CD4 T lymphocyte lineage-specification in mice. To our knowledge, this is the first in vivo demonstration of functional equivalency for a silencer element between marsupial and placental mammals using a definitive knockin approach. Finally, we show that alteration of the position/orientation of a highly conserved region within the murine Sil^ThPOK is sufficient to destroy silencer activity in vivo, demonstrating that motif grammar of this “solid” synteny block is critical for silencer function. Dependence of Sil^ThPOK function on motif grammar conserved since the mid-Jurassic age, 165 Ma, suggests that the Sil^ThPOK operates as a silenceosome, by analogy with the previously proposed enhanceosome model.

The Origin of a New Sex Chromosome by Introgression between Two Stickleback Fishes

Mon, 01 Oct 2018 00:00:00 GMT

Introgression is increasingly recognized as a source of genetic diversity that fuels adaptation. Its role in the evolution of sex chromosomes, however, is not well known. Here, we confirm the hypothesis that the Y chromosome in the ninespine stickleback, Pungitius pungitius, was established by introgression from the Amur stickleback, P. sinensis. Using whole genome resequencing, we identified a large region of Chr 12 in P. pungitius that is diverged between males and females. Within but not outside of this region, several lines of evidence show that the Y chromosome of P. pungitius shares a most recent common ancestor not with the X chromosome, but with the homologous chromosome in P. sinensis. Accumulation of repetitive elements and gene expression changes on the new Y are consistent with a young sex chromosome in early stages of degeneration, but other hallmarks of Y chromosomes have not yet appeared. Our findings indicate that porous species boundaries can trigger rapid sex chromosome evolution.