Nature, Science, Cell, PNAS, PLoS Biology, eLife, Current Biology, Genetics, Evolution, Development Machine behaviour Iyad Rahwan, Manuel Cebrian, Nick Obradovich, Josh Bongard, Jean-François Bonnefon, Cynthia Breazeal, Jacob W. Crandall, Nicholas A. Christakis, Iain D. Couzin, Matthew O. Jackson, Nicholas R. Jennings, Ece Kamar, Isabel M. Kloumann, Hugo Larochelle, David Lazer, Richard McElreath, Alan Mislove, David C. Parkes, Alex ‘Sandy’ Pentland, Margaret E. Roberts, Azim Shariff, Joshua B. Tenenbaum & Michael Wellman Nature volume 568, pages 477–486 (2019) Abstract Machines powered by artificial intelligence increasingly mediate our social, cultural, economic and political interactions. Understanding the behaviour of artificial intelligence systems is essential to our ability to control their actions, reap their benefits and minimize their harms. Here we argue that this necessitates a broad scientific research agenda to study machine behaviour that incorporates and expands upon the discipline of computer science and includes insights from across the sciences. We first outline a set of questions that are fundamental to this emerging field and then explore the technical, legal and institutional constraints on the study of machine behaviour. Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula Oliver Jäckle, Brandon K. B. Seah, Målin Tietjen, Nikolaus Leisch, Manuel Liebeke, Manuel Kleiner, Jasmine S. Berg, and Harald R. Gruber-Vodicka PNAS April 23, 2019 116 (17) 8505-8514; first published April 8, 2019 https://doi.org/10.1073/pnas.1818995116 Edited by Margaret J. McFall-Ngai, University of Hawaii at Manoa, Honolulu, HI, and approved March 1, 2019 (received for review November 7, 2018) Abstract Hosts of chemoautotrophic bacteria typically have much higher biomass than their symbionts and consume symbiont cells for nutrition. In contrast to this, chemoautotrophic Candidatus Riegeria symbionts in mouthless Paracatenula flatworms comprise up to half of the biomass of the consortium. Each species of Paracatenula harbors a specific Ca. Riegeria, and the endosymbionts have been vertically transmitted for at least 500 million years. Such prolonged strict vertical transmission leads to streamlining of symbiont genomes, and the retained physiological capacities reveal the functions the symbionts provide to their hosts. Here, we studied a species of Paracatenula from Sant’Andrea, Elba, Italy, using genomics, gene expression, imaging analyses, as well as targeted and untargeted MS. We show that its symbiont, Ca. R. santandreae has a drastically smaller genome (1.34 Mb) than the symbiont´s free-living relatives (4.29–4.97 Mb) but retains a versatile and energy-efficient metabolism. It encodes and expresses a complete intermediary carbon metabolism and enhanced carbon fixation through anaplerosis and accumulates massive intracellular inclusions such as sulfur, polyhydroxyalkanoates, and carbohydrates. Compared with symbiotic and free-living chemoautotrophs, Ca. R. santandreae’s versatility in energy storage is unparalleled in chemoautotrophs with such compact genomes. Transmission EM as well as host and symbiont expression data suggest that Ca. R. santandreae largely provisions its host via outer-membrane vesicle secretion. With its high share of biomass in the symbiosis and large standing stocks of carbon and energy reserves, it has a unique role for bacterial symbionts—serving as the primary energy storage for its animal host. Attachment of the blastoderm to the vitelline envelope affects gastrulation of insects Stefan Münster, Akanksha Jain, Alexander Mietke, Anastasios Pavlopoulos, Stephan W. Grill & Pavel Tomancak Nature volume 568, pages 395–399 (2019) Abstract During gastrulation, physical forces reshape the simple embryonic tissue to form the complex body plans of multicellular organisms1. These forces often cause large-scale asymmetric movements of the embryonic tissue2,3. In many embryos, the gastrulating tissue is surrounded by a rigid protective shell4. Although it is well-recognized that gastrulation movements depend on forces that are generated by tissue-intrinsic contractility5,6, it is not known whether interactions between the tissue and the protective shell provide additional forces that affect gastrulation. Here we show that a particular part of the blastoderm tissue of the red flour beetle (Tribolium castaneum) tightly adheres in a temporally coordinated manner to the vitelline envelope that surrounds the embryo. This attachment generates an additional force that counteracts tissue-intrinsic contractile forces to create asymmetric tissue movements. This localized attachment depends on an αPS2 integrin (inflated), and the knockdown of this integrin leads to a gastrulation phenotype that is consistent with complete loss of attachment. Furthermore, analysis of another integrin (the αPS3 integrin, scab) in the fruit fly (Drosophila melanogaster) suggests that gastrulation in this organism also relies on adhesion between the blastoderm and the vitelline envelope. Our findings reveal a conserved mechanism through which the spatiotemporal pattern of tissue adhesion to the vitelline envelope provides controllable, counteracting forces that shape gastrulation movements in insects. Genetic paradox explained by nonsense Miles F. Wilkinson Nature NEWS AND VIEWS 03 April 2019 Gene mutations that truncate the encoded protein can trigger the expression of related genes. The discovery of this compensatory response changes how we think about genetic studies in humans and model organisms. Convergent regulatory evolution and loss of flight in paleognathous birds Timothy B. Sackton1,2,*, Phil Grayson2,3, Alison Cloutier2,3, Zhirui Hu4, Jun S. Liu4, Nicole E. Wheeler5,6, Paul P. Gardner5,7, Julia A. Clarke8, Allan J. Baker9,10, Michele Clamp1, Scott V. Edwards2,3,* Science 05 Apr 2019: Vol. 364, Issue 6435, pp. 74-78 DOI: 10.1126/science.aat7244 Science, this issue p. 74 Abstract A core question in evolutionary biology is whether convergent phenotypic evolution is driven by convergent molecular changes in proteins or regulatory regions. We combined phylogenomic, developmental, and epigenomic analysis of 11 new genomes of paleognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight. A Bayesian analysis of 284,001 conserved noncoding elements, 60,665 of which are corroborated as enhancers by open chromatin states during development, identified 2355 independent accelerations along lineages of flightless paleognaths, with functional consequences for driving gene expression in the developing forelimb. Our results suggest that the genomic landscape associated with morphological convergence in ratites has a substantial shared regulatory component. Rapid plant evolution driven by the interaction of pollination and herbivory Sergio E. Ramos, Florian P. Schiestl* Science 12 Apr 2019: Vol. 364, Issue 6436, pp. 193-196 DOI: 10.1126/science.aav6962 Science, this issue p. 193; see also p. 122 Abstract Pollination and herbivory are both key drivers of plant diversity but are traditionally studied in isolation from each other. We investigated real-time evolutionary changes in plant traits over six generations by using fast-cycling Brassica rapa plants and manipulating the presence and absence of bumble bee pollinators and leaf herbivores. We found that plants under selection by bee pollinators evolved increased floral attractiveness, but this process was compromised by the presence of herbivores. Plants under selection from both bee pollinators and herbivores evolved higher degrees of self-compatibility and autonomous selfing, as well as reduced spatial separation of sexual organs (herkogamy). Overall, the evolution of most traits was affected by the interaction of bee pollination and herbivory, emphasizing the importance of the cross-talk between both types of interactions for plant evolution. Unbiased detection of CRISPR off-targets in vivo using DISCOVER-Seq Beeke Wienert1,2,3,*, Stacia K. Wyman1,*, Christopher D. Richardson1,2, Charles D. Yeh1,2,†, Pinar Akcakaya4, Michelle J. Porritt4, Michaela Morlock4, Jonathan T. Vu1, Katelynn R. Kazane1,2, Hannah L. Watry1,3, Luke M. Judge3,5, Bruce R. Conklin3,6, Marcello Maresca4, Jacob E. Corn1,2,†,‡ Science 19 Apr 2019: Vol. 364, Issue 6437, pp. 286-289 DOI: 10.1126/science.aav9023 Science, this issue p. 286, p. 289, p. 292; see also p. 234 Abstract CRISPR-Cas genome editing induces targeted DNA damage but can also affect off-target sites. Current off-target discovery methods work using purified DNA or specific cellular models but are incapable of direct detection in vivo. We developed DISCOVER-Seq (discovery of in situ Cas off-targets and verification by sequencing), a universally applicable approach for unbiased off-target identification that leverages the recruitment of DNA repair factors in cells and organisms. Tracking the precise recruitment of MRE11 uncovers the molecular nature of Cas activity in cells with single-base resolution. DISCOVER-Seq works with multiple guide RNA formats and types of Cas enzymes, allowing characterization of new editing tools. Off-targets can be identified in cell lines and patient-derived induced pluripotent stem cells and during adenoviral editing of mice, paving the way for in situ off-target discovery within individual patient genotypes during therapeutic genome editing. Growth and morphogenesis of the gastropod shell Adam B. Johnson, Nina S. Fogel, and J. David Lambert PNAS April 2, 2019 116 (14) 6878-6883; first published March 13, 2019 https://doi.org/10.1073/ Edited by Günter P. Wagner, Yale University, New Haven, CT, and approved February 1, 2019 (received for review September 18, 2018) Abstract Gastropod shell morphologies are famously diverse but generally share a common geometry, the logarithmic coil. Variations on this morphology have been modeled mathematically and computationally but the developmental biology of shell morphogenesis remains poorly understood. Here we characterize the organization and growth patterns of the shell-secreting epithelium of the larval shell of the basket whelk Tritia (also known as Ilyanassa). Despite the larval shell’s relative simplicity, we find a surprisingly complex organization of the shell margin in terms of rows and zones of cells. We examined cell division patterns with EdU incorporation assays and found two growth zones within the shell margin. In the more anterior aperture growth zone, we find that inferred division angles are biased to lie parallel to the shell edge, and these divisions occur more on the margin’s left side. In the more posterior mantle epithelium growth zone, inferred divisions are significantly biased to the right, relative to the anterior–posterior axis. These growth zones, and the left–right asymmetries in cleavage patterns they display, can explain the major modes of shell morphogenesis at the level of cellular behavior. In a gastropod with a different coiling geometry, Planorbella sp., we find similar shell margin organization and growth zones as Tritia, but different left–right asymmetries than we observed in the helically coiled shell of Tritia. These results indicate that differential growth patterns in the mantle edge epithelium contribute to shell shape in gastropod shells and identify cellular mechanisms that may vary to generate shell diversity in evolution. Transposable elements drive rapid phenotypic variation in Capsella rubella Xiao-Min Niu, Yong-Chao Xu, Zi-Wen Li, Yu-Tao Bian, Xing-Hui Hou, Jia-Fu Chen, Yu-Pan Zou, Juan Jiang, Qiong Wu, Song Ge, Sureshkumar Balasubramanian, and Ya-Long Guo PNAS April 2, 2019 116 (14) 6908-6913; first published March 15, 2019 https://doi.org/10.1073/pnas.1811498116 Edited by Ian T. Baldwin, Max Planck Institute for Chemical Ecology, Jena, Germany, and approved February 19, 2019 (received for review July 4, 2018) Abstract Rapid phenotypic changes in traits of adaptive significance are crucial for organisms to thrive in changing environments. How such phenotypic variation is achieved rapidly, despite limited genetic variation in species that experience a genetic bottleneck is unknown. Capsella rubella, an annual and inbreeding forb (Brassicaceae), is a great system for studying this basic question. Its distribution is wider than those of its congeneric species, despite an extreme genetic bottleneck event that severely diminished its genetic variation. Here, we demonstrate that transposable elements (TEs) are an important source of genetic variation that could account for its high phenotypic diversity. TEs are (i) highly enriched in C. rubella compared with its outcrossing sister species Capsella grandiflora, and (ii) 4.2% of polymorphic TEs in C. rubella are associated with variation in the expression levels of their adjacent genes. Furthermore, we show that frequent TE insertions at FLOWERING LOCUS C (FLC) in natural populations of C. rubella could explain 12.5% of the natural variation in flowering time, a key life history trait correlated with fitness and adaptation. In particular, we show that a recent TE insertion at the 3′ UTR of FLC affects mRNA stability, which results in reducing its steady-state expression levels, to promote the onset of flowering. Our results highlight that TE insertions can drive rapid phenotypic variation, which could potentially help with adaptation to changing environments in a species with limited standing genetic variation. Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes Richard G. Dorrell, Tomonori Azuma, Mami Nomura, Guillemette Audren de Kerdrel, Lucas Paoli, Shanshan Yang, Chris Bowler, Ken-ichiro Ishii, Hideaki Miyashita, Gillian H. Gile, and Ryoma Kamikawa PNAS April 2, 2019 116 (14) 6914-6923; first published March 14, 2019 https://doi.org/10.1073/ Edited by John M. Archibald, Dalhousie University, Halifax, NS, Canada, and accepted by Editorial Board Member W. F. Doolittle February 19, 2019 (received for review November 22, 2018) Abstract The division of life into producers and consumers is blurred by evolution. For example, eukaryotic phototrophs can lose the capacity to photosynthesize, although they may retain vestigial plastids that perform other essential cellular functions. Chrysophyte algae have undergone a particularly large number of photosynthesis losses. Here, we present a plastid genome sequence from a nonphotosynthetic chrysophyte, “Spumella” sp. NIES-1846, and show that it has retained a nearly identical set of plastid-encoded functions as apicomplexan parasites. Our transcriptomic analysis of 12 different photosynthetic and nonphotosynthetic chrysophyte lineages reveals remarkable convergence in the functions of these nonphotosynthetic plastids, along with informative lineage-specific retentions and losses. At one extreme, Cornospumella fuschlensis retains many photosynthesis-associated proteins, although it appears to have lost the reductive pentose phosphate pathway and most plastid amino acid metabolism pathways. At the other extreme, Paraphysomonas lacks plastid-targeted proteins associated with gene expression and all metabolic pathways that require plastid-encoded partners, indicating a complete loss of plastid DNA in this genus. Intriguingly, some of the nucleus-encoded proteins that once functioned in the expression of the Paraphysomonas plastid genome have been retained. These proteins were likely to have been dual targeted to the plastid and mitochondria of the chrysophyte ancestor, and are uniquely targeted to the mitochondria in Paraphysomonas. Our comparative analyses provide insights into the process of functional reduction in nonphotosynthetic plastids. Exaggerated heterochiasmy in a fish with sex-linked male coloration polymorphisms Roberta Bergero, Jim Gardner, Beth Bader, Lengxob Yong, and Deborah Charlesworth PNAS April 2, 2019 116 (14) 6924-6931; first published March 20, 2019 https://doi.org/10.1073/ Edited by Michael Lynch, Arizona State University, Tempe, AZ, and approved February 19, 2019 (received for review October 31, 2018) Abstract It is often stated that polymorphisms for mutations affecting fitness of males and females in opposite directions [sexually antagonistic (SA) polymorphisms] are the main selective force for the evolution of recombination suppression between sex chromosomes. However, empirical evidence to discriminate between different hypotheses is difficult to obtain. We report genetic mapping results in laboratory-raised families of the guppy (Poecilia reticulata), a sexually dimorphic fish with SA polymorphisms for male coloration genes, mostly on the sex chromosomes. Comparison of the genetic and physical maps shows that crossovers are distributed very differently in the two sexes (heterochiasmy); in male meiosis, they are restricted to the termini of all four chromosomes studied, including chromosome 12, which carries the sex-determining locus. Genome resequencing of male and female guppies from a population also indicates sex linkage of variants across almost the entire chromosome 12. More than 90% of the chromosome carrying the male-determining locus is therefore transmitted largely through the male lineage. A lack of heterochiasmy in a related fish species suggests that it originated recently in the lineage leading to the guppy. Our findings do not support the hypothesis that suppressed recombination evolved in response to the presence of SA polymorphisms. Instead, a low frequency of recombination on a chromosome that carries a male-determining locus and has not undergone genetic degeneration has probably facilitated the establishment of male-beneficial coloration polymorphisms. Disease mortality in domesticated animals is predicted by host evolutionary relationships Maxwell J. Farrell and T. Jonathan Davies PNAS April 16, 2019 116 (16) 7911-7915; first published March 29, 2019 https://doi.org/10.1073/ Edited by Douglas Futuyma, Stony Brook University, Stony Brook, NY, and approved February 28, 2019 (received for review October 8, 2018) Abstract Infectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multihost parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multihost parasites. Here, using a global dataset of >4,000 case-fatality rates for 65 infectious diseases (caused by microparasites and macroparasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phylogenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts. Sexual conflict drives male manipulation of female postmating responses in Drosophila melanogaster Brian Hollis, Mareike Koppik, Kristina U. Wensing, Hanna Ruhmann, Eléonore Genzoni, Berra Erkosar, Tadeusz J. Kawecki, Claudia Fricke, and Laurent Keller PNAS April 23, 2019 116 (17) 8437-8444; first published April 8, 2019 https://doi.org/10.1073/pnas.1821386116 Edited by Brian Charlesworth, University of Edinburgh, Edinburgh, United Kingdom, and approved March 18, 2019 (received for review December 14, 2018) Abstract In many animals, females respond to mating with changes in physiology and behavior that are triggered by molecules transferred by males during mating. In Drosophila melanogaster, proteins in the seminal fluid are responsible for important female postmating responses, including temporal changes in egg production, elevated feeding rates and activity levels, reduced sexual receptivity, and activation of the immune system. It is unclear to what extent these changes are mutually beneficial to females and males or instead represent male manipulation. Here we use an experimental evolution approach in which females are randomly paired with a single male each generation, eliminating any opportunity for competition for mates or mate choice and thereby aligning the evolutionary interests of the sexes. After >150 generations of evolution, males from monogamous populations elicited a weaker postmating stimulation of egg production and activity than males from control populations that evolved with a polygamous mating system. Males from monogamous populations did not differ from males from polygamous populations in their ability to induce refractoriness to remating in females, but they were inferior to polygamous males in sperm competition. Mating-responsive genes in both the female abdomen and head showed a dampened response to mating with males from monogamous populations. Males from monogamous populations also exhibited lower expression of genes encoding seminal fluid proteins, which mediate the female response to mating. Together, these results demonstrate that the female postmating response, and the male molecules involved in eliciting this response, are shaped by ongoing sexual conflict. Testing the role of trait reversal in evolutionary diversification using song loss in wild crickets Nathan W. Bailey, Sonia Pascoal, and Fernando Montealegre-Z PNAS April 30, 2019 116 (18) 8941-8949; first published April 16, 2019 https://doi.org/10.1073/pnas.1818998116 Edited by Günter P. Wagner, Yale University, New Haven, CT, and approved March 6, 2019 (received for review November 19, 2018) Abstract The mechanisms underlying rapid macroevolution are controversial. One largely untested hypothesis that could inform this debate is that evolutionary reversals might release variation in vestigial traits, which then facilitates subsequent diversification. We evaluated this idea by testing key predictions about vestigial traits arising from sexual trait reversal in wild field crickets. In Hawaiian Teleogryllus oceanicus, the recent genetic loss of sound-producing and -amplifying structures on male wings eliminates their acoustic signals. Silence protects these “flatwing” males from an acoustically orienting parasitoid and appears to have evolved independently more than once. Here, we report that flatwing males show enhanced variation in vestigial resonator morphology under varied genetic backgrounds. Using laser Doppler vibrometry, we found that these vestigial sound-producing wing features resonate at highly variable acoustic frequencies well outside the normal range for this species. These results satisfy two important criteria for a mechanism driving rapid evolutionary diversification: Sexual signal loss was accompanied by a release of vestigial morphological variants, and these could facilitate the rapid evolution of novel signal values. Widespread secondary trait losses have been inferred from fossil and phylogenetic evidence across numerous taxa, and our results suggest that such reversals could play a role in shaping historical patterns of diversification. Exaggeration and cooption of innate immunity for social defense Mayako Kutsukake, Minoru Moriyama, Shuji Shigenobu, Xian-Ying Meng, Naruo Nikoh, Chiyo Noda, Satoru Kobayashi, and Takema Fukatsu PNAS April 30, 2019 116 (18) 8950-8959; first published April 15, 2019 https://doi.org/10.1073/pnas.1900917116 Edited by Nancy A. Moran, University of Texas at Austin, Austin, TX, and approved March 14, 2019 (received for review January 17, 2019) Abstract Social insects often exhibit striking altruistic behaviors, of which the most spectacular ones may be self-destructive defensive behaviors called autothysis, “self-explosion,” or “suicidal bombing.” In the social aphid Nipponaphis monzeni, when enemies damage their plant-made nest called the gall, soldier nymphs erupt to discharge a large amount of body fluid, mix the secretion with their legs, and skillfully plaster it over the plant injury. Dozens of soldiers come out, erupt, mix, and plaster, and the gall breach is promptly sealed with the coagulated body fluid. What molecular and cellular mechanisms underlie the self-sacrificing nest repair with body fluid for the insect society? Here we demonstrate that the body cavity of soldier nymphs is full of highly differentiated large hemocytes that contain huge amounts of lipid droplets and phenoloxidase (PO), whereas their hemolymph accumulates huge amounts of tyrosine and a unique repeat-containing protein (RCP). Upon breakage of the gall, soldiers gather around the breach and massively discharge the body fluid. The large hemocytes rupture and release lipid droplets, which promptly form a lipidic clot, and, concurrently, activated PO converts tyrosine to reactive quinones, which cross-link RCP and other macromolecules to physically reinforce the clot to seal the gall breach. Here, soldiers’ humoral and cellular immune mechanisms for wound sealing are extremely up-regulated and utilized for colony defense, which provides a striking case of direct evolutionary connection between individual immunity and social immunity and highlights the importance of exaggeration and cooption of preexisting traits to create evolutionary novelties. Genome-wide sexually antagonistic variants reveal long-standing constraints on sexual dimorphism in fruit flies Filip Ruzicka , Mark S. Hill , Tanya M. Pennell , Ilona Flis, Fiona C. Ingleby, Richard Mott, Kevin Fowler, Edward H. Morrow , Max Reuter PLOS Published: April 25, 2019 https://doi.org/10.1371/journal.pbio.3000244 Abstract The evolution of sexual dimorphism is constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location, and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identify approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range and in their sister species D. simulans, indicating widespread and evolutionarily persistent (about 1 million years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation. A novel evolutionary conserved mechanism of RNA stability regulates synexpression of primordial germ cell-specific genes prior to the sex-determination stage in medaka Amaury Herpin , Cornelia Schmidt, Susanne Kneitz, Clara Gobé, Martina Regensburger, Aurélie Le Cam, Jérome Montfort, Mateus C. Adolfi, Christina Lillesaar, Dagmar Wilhelm, Michael Kraeussling , Brigitte Mourot, Béatrice Porcon, [ ... ], Manfred Schartl [ view all ] PLOS Published: April 4, 2019 https://doi.org/10.1371/journal.pbio.3000185 Abstract Dmrt1 is a highly conserved transcription factor, which is critically involved in regulation of gonad development of vertebrates. In medaka, a duplicate of dmrt1—acting as master sex-determining gene—has a tightly timely and spatially controlled gonadal expression pattern. In addition to transcriptional regulation, a sequence motif in the 3′ UTR (D3U-box) mediates transcript stability of dmrt1 mRNAs from medaka and other vertebrates. We show here that in medaka, two RNA-binding proteins with antagonizing properties target this D3U-box, promoting either RNA stabilization in germ cells or degradation in the soma. The D3U-box is also conserved in other germ-cell transcripts, making them responsive to the same RNA binding proteins. The evolutionary conservation of the D3U-box motif within dmrt1 genes of metazoans—together with preserved expression patterns of the targeting RNA binding proteins in subsets of germ cells—suggest that this new mechanism for controlling RNA stability is not restricted to fishes but might also apply to other vertebrates. Bichir external gills arise via heterochronic shift that accelerates hyoid arch development Jan Stundl, Anna Pospisilova, David Jandzik, Peter Fabian, Barbora Dobiasova, Martin Minarik, Brian D Metscher, Vladimir Soukup Is a corresponding author , Robert Cerny Is a corresponding author Research Article Mar 26, 2019 eLife 2019;8:e43531 doi: 10.7554/eLife.43531 Abstract In most vertebrates, pharyngeal arches form in a stereotypic anterior-to-posterior progression. To gain insight into the mechanisms underlying evolutionary changes in pharyngeal arch development, here we investigate embryos and larvae of bichirs. Bichirs represent the earliest diverged living group of ray-finned fishes, and possess intriguing traits otherwise typical for lobe-finned fishes such as ventral paired lungs and larval external gills. In bichir embryos, we find that the anteroposterior way of formation of cranial segments is modified by the unique acceleration of the entire hyoid arch segment, with earlier and orchestrated development of the endodermal, mesodermal, and neural crest tissues. This major heterochronic shift in the anteroposterior developmental sequence enables early appearance of the external gills that represent key breathing organs of bichir free-living embryos and early larvae. Bichirs thus stay as unique models for understanding developmental mechanisms facilitating increased breathing capacity. https://doi.org/10.7554/eLife.43531.001 Genome Size Evolution: Small Transposons with Large Consequences Alexander Suh Current Biology Volume 29, ISSUE 7, PR241-R243, April 01, 2019 DOI:https://doi.org/10.1016/j.cub.2019.02.032 Transposable elements (TEs) heavily influence genome size variation between organisms. A new study on larvacean tunicates now shows that even non-autonomous TEs — small TEs that parasitize the enzymatic machinery of large, autonomous TEs — can have a large impact on genome size. Behavior: Why Male Flies Sing Different Songs Dana S. Galili Gregory S.X.E. Jefferis Current Biology | Volume 29, ISSUE 7, PR243-R245, April 01, 2019 DOI:https://doi.org/10.1016/j.cub.2019.02.054 A new study investigates the distinct male courtship songs of two related Drosophila species and the neurons controlling this behavior, localizing a site of evolutionary divergence to the motor system, downstream of the central brain. Drosophila Courtship: Neuronal Coordination of Behavioural Sequences and a 60-Year-Old Hypothesis Matthew Cobb Current Biology| Volume 29, ISSUE 7, PR250-R252, April 01, 2019 DOI:https://doi.org/10.1016/j.cub.2019.02.030 Drosophila courtship consists of a stereotypic sequence of behaviours, involving increasing levels of excitation. A pair of neurons coordinate some of these sequences using a spike-counting model that echoes an idea first outlined in 1959. Neural Evolution of Context-Dependent Fly Song Yun Ding 3 Joshua L. Lillvis 3 Jessica Cande Gordon J. Berman Benjamin J. Arthur Xi Long Min Xu Barry J. Dickson David L. Stern Article| Volume 29, ISSUE 7, P1089-1099.e7, April 01, 2019 2019DOI:https://doi.org/10.1016/j.cub.2019.02.019 Highlights • Genetic reagents target homologous neurons in multiple Drosophila species • Homologous descending neurons drive distinct fly songs in a similar social context • Evolutionary changes downstream of the homologous neurons cause song differences • Courtship song circuit multifunctionality may facilitate rapid fly song evolution Summary It is unclear where in the nervous system evolutionary changes tend to occur. To localize the source of neural evolution that has generated divergent behaviors, we developed a new approach to label and functionally manipulate homologous neurons across Drosophila species. We examined homologous descending neurons that drive courtship song in two species that sing divergent song types and localized relevant evolutionary changes in circuit function downstream of the intrinsic physiology of these descending neurons. This evolutionary change causes different species to produce divergent motor patterns in similar social contexts. Artificial stimulation of these descending neurons drives multiple song types, suggesting that multifunctional properties of song circuits may facilitate rapid evolution of song types. Massive Changes of Genome Size Driven by Expansions of Non-autonomous Transposable Elements Magali Naville 5 Simon Henriet 5 Ian Warren Magnus Reeve 4 Jean-Nicolas Volff Daniel Chourrout 6 Current Biology| Volume 29, ISSUE 7, P1161-1168.e6, April 01, 2019 Published:March 14, 2019DOI:https://doi.org/10.1016/j.cub.2019.01.080 Highlights • Genome size varies up to 12× in larvaceans, chordates with a distinctive anatomy • Small and large species have the smallest and largest genomes, respectively • Transposable elements have driven multiple independent genome expansions • Genomes mainly increased through accumulations of non-autonomous elements (SINEs) Summary In eukaryotes, genome size correlates little with the number of coding genes or the level of organismal complexity (C-value paradox). The underlying causes of variations in genome size, whether adaptive or neutral, remain unclear, although several biological traits often covary with it [ 1, 2, 3, 4, 5]. Rapid increases in genome size occur mainly through whole-genome duplications or bursts in the activity of transposable elements (TEs) [ 6]. The very small and compact genome of Oikopleura dioica, a tunicate of the larvacean class, lacks elements of most ancient families of animal retrotransposons [ 7, 8]. Here, we sequenced the genomes of six other larvaceans, all of which are larger than that of Oikopleura (up to 12 times) and which increase in size with greater body length. Although no evidence was found for whole-genome duplications within the group of species, the global amount of TEs strongly correlated with genome size. Compared to other metazoans, however, the TE diversity was reduced in all species, as observed previously in O. dioica, suggesting a common ancestor with a compacted genome. Strikingly, non-autonomous elements, particularly short interspersed nuclear elements (SINEs), massively contributed to genome size variation through species-specific independent amplifications, ranging from 3% in the smallest genome up to 49% in the largest. Variations in SINE abundance explain as much as 83% of interspecific genome size variation. These data support an indirect influence of autonomous TEs on genome size via their ability to mobilize non-autonomous elements. Joint Evolution of Asexuality and Queen Number in an Ant Kip D. Lacy 3, 4 DeWayne Shoemaker Kenneth G. Ross Current Biology | Volume 29, ISSUE 8, P1394-1400.e4, April 22, 2019 Published:April 11, 2019DOI:https://doi.org/10.1016/j.cub.2019.03.018 Highlights • Multi-queen colonies of a fire ant produce queens asexually but workers sexually • Single-queen colonies produce both queens and workers sexually • Queens in multi-queen colonies require sperm from single-queen colony males to produce workers • Distinct asexual/multi-queen lineages may stem from a sexual/single-queen population Summary Ants exhibit a striking diversity of reproductive systems, varying in traits such as the number of reproductives per colony [ 1], the mode of daughter production (sexual or asexual) [ 2], and the mode of caste determination (genetic or environmental) [ 3]. Species employing mixed reproductive systems present a unique opportunity to explore the causes and consequences of alternative breeding strategies. Mixed reproductive systems in ants include social polymorphism in colony queen number, whereby single-queen (monogyne) and multiple-queen (polygyne) colonies co-occur within species [ 4, 5, 6, 7], and facultative asexuality, in which female offspring may be produced sexually or asexually within colonies [ 8, 9, 10, 11, 12, 13]. Here, we document a remarkable confluence of multiple mixed reproductive systems in the tropical fire ant, Solenopsis geminata, in a population with three important features: (1) polygyne colonies produce workers sexually but queens asexually, whereas monogyne colonies produce both castes sexually; (2) polygyne queens mate with monogyne males to produce workers, but monogyne queens do not mate with polygyne males; and (3) different asexual/polygyne lineages evidently were founded separately by genetically distinct founder queens, which appear to have originated from the same neighboring monogyne population. Multiple asexual/polygyne genomes are transmitted undiluted in this system, but sterile workers produced with sperm from a sexually-reproducing/monogyne population are necessary for the persistence of these lineages. The intersection of social polymorphism, facultative asexuality, and genetic caste determination marks this population of S. geminata as an embodiment of the diversity of ant reproductive systems and suggests previously unknown connections between these phenomena. Multiple Pathways Act Together To Establish Asymmetry of the Ventral Nerve Cord in Caenorhabditis elegans Jesse Taylor and Harald Hutter Genetics April 1, 2019 vol. 211 no. 4 1331-1343; https://doi.org/10.1534/genetics.119.301999 Abstract The central nervous system of most animals is bilaterally symmetrical. Closer observation often reveals some functional or anatomical left–right asymmetries. In the nematode Caenorhabditis elegans, the most obvious asymmetry in the nervous system is found in the ventral nerve cord (VNC), where most axons are in the right axon tract. The asymmetry is established when axons entering the VNC from the brain switch from the left to the right side at the anterior end of the VNC. In genetic screens we identified several mutations compromising VNC asymmetry. This includes alleles of col-99 (encoding a transmembrane collagen), unc-52/perlecan and unc-34 (encoding the actin modulator Enabled/Vasodilator-stimulated phosphoproteins). In addition, we evaluated mutants in known axon guidance pathways for asymmetry defects and used genetic interaction studies to place the genes into genetic pathways. In total we identified four different pathways contributing to the establishment of VNC asymmetry, represented by UNC-6/netrin, SAX-3/Robo, COL-99, and EPI-1/laminin. The combined inactivation of these pathways in triple and quadruple mutants leads to highly penetrant VNC asymmetry defects, suggesting these pathways are important contributors to the establishment of VNC asymmetry in C. elegans. A Multivariate Genome-Wide Association Study of Wing Shape in Drosophila melanogaster William Pitchers, Jessica Nye, Eladio J. Márquez, Alycia Kowalski, Ian Dworkin and David Houle Genetics April 1, 2019 vol. 211 no. 4 1429-1447; https://doi.org/10.1534/genetics.118.301342 Abstract Due to the complexity of genotype–phenotype relationships, simultaneous analyses of genomic associations with multiple traits will be more powerful and informative than a series of univariate analyses. However, in most cases, studies of genotype–phenotype relationships have been analyzed only one trait at a time. Here, we report the results of a fully integrated multivariate genome-wide association analysis of the shape of the Drosophila melanogaster wing in the Drosophila Genetic Reference Panel. Genotypic effects on wing shape were highly correlated between two different laboratories. We found 2396 significant SNPs using a 5% false discovery rate cutoff in the multivariate analyses, but just four significant SNPs in univariate analyses of scores on the first 20 principal component axes. One quarter of these initially significant SNPs retain their effects in regularized models that take into account population structure and linkage disequilibrium. A key advantage of multivariate analysis is that the direction of the estimated phenotypic effect is much more informative than a univariate one. We exploit this fact to show that the effects of knockdowns of genes implicated in the initial screen were on average more similar than expected under a null model. A subset of SNP effects were replicable in an unrelated panel of inbred lines. Association studies that take a phenomic approach, considering many traits simultaneously, are an important complement to the power of genomics. The evolution of eye size in response to increased fish predation in Daphnia Shannon M. Beston Jeffry L. Dudycha David M. Post Matthew R. Walsh Evolution Volume73, Issue4 April 2019 Pages 792-802 First published: 07 March 2019 https://doi.org/10.1111/evo.13717 Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator‐induced mortality has recently been identified as a potential driver of eye size variation. Here, we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild‐caught and third‐generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild‐caught specimens did not differ in eye size across all lakes. However, third‐generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size. Research Highlight Left-right asymmetry: diaphanous decisively determines dextral Development 2019 146: e0905 Masanori Abe, Reiko Kuroda vol. 146 no. 9, e0905 Left-right asymmetry is pervasive in animals and known to be under tight genetic control. One conspicuous example is in snails: their shells coil either dextrally (as in most species or strains within a species) or sinistrally, and the shell reflects the chirality of the whole body, which is established in early embryogenesis. Previous work has implicated the formin diaphanous in the regulation of chirality in Lymnaea snails, but it was unclear whether Lsdia1 was truly the causative gene, or just linked to it. Now, Masanori Abe and Reiko Kuroda provide definitive proof of the role of Lsdia1 in shell coiling. CRISPR/Cas9 targeting of Lsdia1 leads to sinistral offspring in a dextral background, in a stably inherited manner. In the embryo, LsDia1 regulates the third cleavage, when definitive chirality is first displayed. Mothers with Lsdia1 mutations produced embryos that, at the one-cell stage, lacked detectable LsDia1 protein. Remarkably, reducing vitelline membrane tension reveals that the fertilised egg itself shows chirality, and that this depends on the Lsdia1 genotype of the mother. Finally, sinistral embryos show mirror-image patterns of nodal and Pitx expression, two genes known to regulate chirality across animals. This study thus reports the first CRISPR/Cas9 gene knockouts in molluscs, the earliest demonstration of chirality in animals, and decisively proves the contribution of LsDia1 to LR patterning in Lymnaea.