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Background During evolution, genes can experience duplications, losses, inversions and gene conversions. Why certain genes are more dynamic than others is poorly understood. Here we examine how several Sgs genes encoding glue proteins, which make up a bioadhesive that sticks the animal during metamorphosis, have evolved in Drosophila species. Results We examined high-quality genome assemblies of 24 Drosophila species to study the evolutionary dynamics of the Sgs1-Sgs3-Sgs7-Sgs8 family glue genes at an unprecedented resolution across approximately 30 millions of years. A total of 102 Sgs genes were annotated and grouped into 4 subfamilies. We present here a new nomenclature for Sgs genes based on protein sequence conservation, genomic location and presence/absence of internal repeats. Two types of glue genes were uncovered. The first category (Sgs1, Sgs3X, Sgs3e) experienced a few gene losses but no duplication, no local inversion and no gene conversion. The second group (Sgs3b, Sgs7, Sgs8) exhibited multiple events of gene losses, gene duplications, local inversions and gene conversions. Our data suggest that the presence of short "new glue" genes near the genes of the latter group may have accelerated their dynamics. Conclusions Our comparative analysis suggests that the evolutionary dynamics of glue genes is influenced by genomic context. Our molecular, phylogenetic and comparative analysis of the glue gene family Sgs1-Sgs3-Sgs7-Sgs8 provides the foundation for investigating the role of the various glue genes during Drosophila life.

Insects are important elements of terrestrial ecosystems because they pollinate plants, destroy crops, transmit diseases to livestock and humans, and are important components of food chains. Here I used Gephebase, a manually curated database of genetic variants associated with natural and domesticated trait variation, to explore current knowledge about the genes and the mutations known to contribute to natural phenotypic variation in insects. Analysis of over 600 mutations reveals that data are concentrated towards certain species and traits and that experimental approaches have changed over time. The distribution of coding and cis-regulatory changes varies with traits, experimental approaches and identified gene loci. Recent studies highlight the important role of standing variation, repeated mutations in hotspot genes, recombination, inversions, and introgression.HighlightsGephebase compiles more than 600 genes and mutations contributing to insect natural variationOur genetic knowledge is biased towards certain traits and insect speciesExperimental approaches and studied insect species have changed over the yearsThe relative distribution of coding and cis-regulatory mutations varies with traits and genesClusters of causal mutations are more frequently found in insects than in other organisms

Male genitalia are usually extremely divergent between closely related species, but relatively constant within one species. Here we examine the effect of temperature on the shape of the ventral branches, a male genital structure involved in reproductive isolation, in the sister species Drosophila santomea and Drosophila yakuba. We designed a semi‐automatic measurement machine learning pipeline that can reliably identify curvatures and landmarks based on manually digitized contours of the ventral branches. With this method, we observed that temperature does not affect ventral branches in D. yakuba but that in D. santomea ventral branches tend to morph into a D. yakuba‐like shape at lower temperature. We found that male genitalia structures involved in reproductive isolation can be relatively variable within one species and can resemble the shape of closely related species’ genitalia through plasticity to temperature. Our results suggest that reproductive isolation mechanisms can be dependent on the environmental context., The closely related species Drosophila yakuba and Drosophila santomea have distinctive ventral branches, a male genital structure involved in reproductive isolation. We designed a semi‐automatic method to measure the shape of the ventral branches and found that temperature does not affect ventral branches in D. yakuba but that in D. santomea ventral branches tend to morph into a D. yakuba‐like shape at lower temperature. ​

Does evolution proceed in small steps or large leaps? How repeatable is evolution? How constrained is the evolutionary process? Answering these long-standing questions in evolutionary biology is indispensable for both understanding how extant biodiversity has evolved and predicting how organisms and ecosystems will respond to changing environments in the future. Understanding the genetic basis of phenotypic diversification and speciation in natural populations is key to properly answering these questions. The leap forward in genome sequencing technologies has made it increasingly easier to not only investigate the genetic architecture but also identify the variant sites underlying adaptation and speciation in natural populations. Furthermore, recent advances in genome editing technologies are making it possible to investigate the functions of each candidate gene in organisms from natural populations. In this article, we discuss how these recent technological advances enable the analysis of causative genes and mutations and how such analysis can help answer long-standing evolutionary biology questions. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’.

The model organism Drosophila melanogaster has become a focal system for investigations of rapidly evolving genital morphology as well as the development and functions of insect reproductive structures. To follow up on a previous paper outlining unifying terminology for the structures of the male terminalia in this species, we offer here a detailed description of the female terminalia of D. melanogaster. Informative diagrams and micrographs are presented to provide a comprehensive overview of the external and internal reproductive structures of females. We propose a collection of terms and definitions to standardize the terminology associated with the female terminalia in D. melanogaster and we provide a correspondence table with the terms previously used. Unifying terminology for both males and females in this species will help to facilitate communication between various disciplines, as well as aid in synthesizing research across publications within a discipline that has historically focused principally on male features. Our efforts to refine and standardize the terminology should expand the utility of this important model system for addressing questions related to the development and evolution of animal genitalia, and morphology in general.

Left-right asymmetries recurrently evolve in animals but the underlying developmental mechanisms are unknown. In mostDrosophilaspecies, the male genitalia is symmetric and undergoes a clockwise 360° rotation during development. InD. melanogaster, this tissue remodeling process is directed by class I myosins: in MyoID mutants the rotation is reversed and the genitalia remains symmetric. Males ofDrosophila pacheahave evolved unique left-right asymmetric genital organs and a characteristic right-sided copulation posture in the past 3-6 million years. To test if these asymmetries in morphology and behavior evolved via the recruitment of pre-existing directional cues controlled by MyoID, we used CRISPR to knockout MyoID inD. pachea. Strikingly, mutant males undergo a reverse genitalia rotation and develop mirror-image asymmetric genitalia, indicating that MyoID controls both the direction of genitalia rotation direction and morphological asymmetry. Although genital asymmetry is reversed, MyoID mutants still adopt a wild-type right-sided copulation posture. Our results show that MyoID and its asymmetry guidance role were recruited for the evolution of a novel left-right asymmetry inD. pacheaand that lateralized copulation behavior is determined by other mechanisms. The evolution of a new left-right organ size asymmetry inD. pacheainvolved recruitment of existing directional cues.

Vertebrate pigmentation patterns are amongst the best characterised model systems for studying the genetic basis of adaptive evolution. The wealth of available data on the genetic basis for pigmentation evolution allows for meta-analysis of trends and quantitative testing of evolutionary hypotheses. We employed Gephebase, a database of genetic variants associated with natural and domesticated trait variation, to examine trends in how cis-regulatory and coding mutations contribute to vertebrate pigmentation phenotypes, as well as factors that favour one mutation type over the other. We found that studies with lower ascertainment bias identified higher proportions of cis-regulatory mutations, and that cis-regulatory mutations were more common amongst animals harboring a higher number of pigment cell classes. We classified pigmentation traits firstly according to their physiological basis and secondly according to whether they affect colour or pattern, and identified that carotenoid-based pigmentation and variation in pattern boundaries are preferentially associated with cis-regulatory change. We also classified genes according to their developmental, cellular, and molecular functions. We found that genes implicated in upstream developmental processes had greater cis-regulatory proportions than downstream cellular function genes, and that ligands were associated with higher cis-regulatory proportions than their respective receptors. Based on these trends, we discuss future directions for research in vertebrate pigmentation evolution.

Molecular evolutionary studies usually focus on genes with clear roles in adult fitness or on developmental genes expressed at multiple time points during the life of the organism. Here, we examine the evolutionary dynamics of Drosophila glue genes, a set of eight genes tasked with a singular primary function during a specific developmental stage: the production of glue that allows animal pupa to attach to a substrate for several days during metamorphosis. Using phenotypic assays and available data from transcriptomics, PacBio genomes, and genetic variation from global populations, we explore the selective forces acting on the glue genes within the cosmopolitan D. melanogaster species and its five closely related species, D. simulans, D. sechellia, D. mauritiana, D. yakuba, and D. teissieri. We observe a three-fold difference in glue adhesion between the least and the most adhesive D. melanogaster strain, indicating a strong genetic component to phenotypic variation. These eight glue genes are among the most highly expressed genes in salivary glands yet they display no notable codon bias. New copies of Sgs3 and Sgs7 are found in D. yakuba and D. teissieri with the Sgs3 coding sequence evolving rapidly after duplication in the D. yakuba branch. Multiple sites along the various glue genes appear to be constrained. Our population genetics analysis in D. melanogaster suggests signs of local adaptive evolution for Sgs3, Sgs5 and Sgs5bis and traces of selective sweeps for Sgs1, Sgs3, Sgs7 and Sgs8. Our work shows that stage-specific genes can be subjected to various dynamic evolutionary forces. (249 words)Significance statementDrosophila larvae produce a glue to stick themselves to a substrate for several days during metamorphosis. Here we observe wide variation in stickiness among Drosophila melanogaster strains and we analyze the molecular evolution of eight glue genes. We find several recent gene duplications and heterogenous rates of evolution among these genes.

Gephebase is a manually-curated database compiling our accumulated knowledge of the genes and mutations that underlie natural, domesticated and experimental phenotypic variation in all Eukaryotes — mostly animals, plants and yeasts. Gephebase aims to compile studies where the genotype-phenotype association (based on linkage mapping, association mapping or a candidate gene approach) is relatively well supported or understood. Human disease and aberrant mutant phenotypes in laboratory model organisms are not included in Gephebase and can be found in other databases (eg. OMIM, OMIA, Monarch Initiative). Gephebase contains more than 1700 entries. Each entry corresponds to an allelic difference at a given gene and its associated phenotypic change(s) between two species or between two individuals of the same species, and is enriched with molecular details, taxonomic information, and bibliographic information. Users can easily browse entries for their topic of interest and perform searches at various levels, whether phenotypic, genetic, taxonomic or bibliographic (eg. transposable elements, cis-regulatory mutations, snakes, carotenoid content, an author name). Data can be searched using keywords and boolean operators and is exportable in spreadsheet format. This database allows to perform meta-analysis to extract general information and global trends about evolution, genetics, and the field of evolutionary genetics itself. Gephebase should also help breeders, conservationists and others to identify the most promising target genes for traits of interest, with potential applications such as crop improvement, parasite and pest control, bioconservation, and genetic diagnostic. It is freely available at www.gephebase.org.

Gene drive and its applications. Gene drive is a new genetic engineering technology that has been developed over the past five years and that allows genetic modifications to spread rapidly in natural populations. Potential applications are numerous, for public health issues, agriculture and conservation biology. This article presents the current developments in this biotechnology, as well as the issues and risks associated with it., Le forçage génétique est une nouvelle technique de manipulation génétique qui a été développée ces cinq dernières années et qui permet de propager rapidement des modifications génétiques dans les populations naturelles. Les applications potentielles sont nombreuses, à la fois en santé publique, en agriculture et en biologie de la conservation. Cet article présente les développements actuels de cette biotechnologie, ainsi que les enjeux et les risques qui y sont associés., Courtier-Orgogozo Virginie. Le forçage génétique (gène drive) et ses applications. In: Bulletin de l'Académie Vétérinaire de France tome 172, 2019. pp. 94-98.

Animals can be permanently attached to a substrate in terrestrial environments at certain stages of their development. Pupa adhesion has evolved multiple times in insects and is thought to maintain the animal in a place where it is not detectable by predators. Here, we investigate whether pupa adhesion in Drosophila can also protect the animal by preventing potential predators from detaching the pupa. We measured the adhesion of Drosophila species sampled from the same area and found that pupa adhesion varies among species, which can be explained by different glue production strategies. Then, we compared attached and manually detached pupae in both field and laboratory assays to investigate the role of pupa adhesion to prevent predation. First, we found that attached pupae remain onsite 30% more than detached pupae in the field after 3 days, probably because they are less predated. Second, we observed that attached pupae are less efficiently predated by ants in the laboratory: they are not carried back to the ant nest and more ants are needed to consume them onsite. Our results show that pupa adhesion can prevent the animal from being taken away by predators and is crucial for Drosophila fly survival.

Genome-scale sequence data have invigorated the study of hybridization and introgression, particularly in animals. However, outside of a few notable cases, we lack systematic tests for introgression at a larger phylogenetic scale across entire clades. Here we leverage 155 genome assemblies, from 149 species, to generate a fossil-calibrated phylogeny and conduct multilocus tests for introgression across nine monophyletic radiations within the genus Drosophila. Using complementary phylogenomic approaches, we identify widespread introgression across the evolutionary history of Drosophila. Mapping gene-tree discordance onto the phylogeny revealed that both ancient and recent introgression has occurred across most of the nine clades that we examined. Our results provide the first evidence of introgression occurring across the evolutionary history of Drosophila and highlight the need to continue to study the evolutionary consequences of hybridization and introgression in this genus and across the Tree of Life.

Introduction Male genitalia are thought to ensure transfer of sperm through direct physical contact with female during copulation. However, little attention has been given to their pre-copulatory role with respect to sexual selection and sexual conflict. Males of the fruitfly Drosophila pachea have a pair of asymmetric external genital lobes, which are primary sexual structures and stabilize the copulatory complex of female and male genitalia. We wondered if genital lobes in D. pachea may have a role before or at the onset of copulation, before genitalia contacts are made. Results We tested this hypothesis with a D. pachea stock where males have variable lobe lengths. In 92 mate competition trials with a single female and two males, females preferentially engaged into a first copulation with males that had a longer left lobe and that displayed increased courtship vigor. In 53 additional trials with both males having partially amputated left lobes of different lengths, we observed a weaker and non-significant effect of left lobe length on copulation success. Courtship durations significantly increased with female age and when two males courted the female simultaneously, compared to trials with only one courting male. In addition, lobe length did not affect sperm transfer once copulation was established. Conclusion Left lobe length affects the chance of a male to engage into copulation. The morphology of this primary sexual trait may affect reproductive success by mediating courtship signals or by facilitating the establishment of genital contacts at the onset of copulation.

CRISPR-based homing gene drive is a genetic control technique aiming to modify or eradicate natural populations. This technique is based on the release of individuals carrying an engineered piece of DNA that can be preferentially inherited by the progeny. Developing countermeasures is important to control the spread of gene drives, should they result in unanticipated damages. One proposed countermeasure is the introduction of individuals carrying a brake construct that targets and inactivates the drive allele but leaves the wild-type allele unaffected. Here we develop models to investigate the efficiency of such brakes. We consider a variable population size and use a combination of analytical and numerical methods to determine the conditions where a brake can prevent the extinction of a population targeted by an eradication drive. We find that a brake is not guaranteed to prevent eradication and that characteristics of both the brake and the drive affect the likelihood of recovering the wild-type population. In particular, brakes that restore fitness are more efficient than brakes that do not. Our model also indicates that threshold-dependent drives (drives that can spread only when introduced above a threshold) are more amenable to control with a brake than drives that can spread from an arbitrary low introduction frequency (threshold-independent drives). Based on our results, we provide practical recommendations and discuss safety issues.Article summary for Issue HighlightsHoming gene drive is a new genetic control technology that aims to spread a genetically engineered DNA construct within natural populations even when it impairs fitness. In case of unanticipated damages, it has been proposed to stop homing gene drives by releasing individuals carrying a genedrive brake; however, the efficiency of such brakes has been little studied. The authors develop a model to investigate the dynamics of a population targeted by a homing drive in absence or in presence of brake. The model provides insights for the design of more efficient brakes and safer gene drives.

Male genitalia are usually extremely divergent between closely related species, but relatively constant within one species. Here we examine the effect of temperature on the shape of the ventral branches, a male genital structure involved in reproductive isolation, in the sister species Drosophila santomea and D. yakuba. We designed a semi-automatic measurement pipeline that can reliably identify curvatures and landmarks based on manually digitized contours of the ventral branches. With this method, we observed that temperature does not affect ventral branches in D. yakuba but that in D. santomea ventral branches tend to morph into a D. yakuba-like shape at lower temperature. Our results suggest that speciation of D. santomea and D. yakuba was associated with a change in genitalia plasticity.

International audience; The Drosophilid fauna has been less investigated in the Atlantic Afrotropical islands than in the Indian Ocean. Located about 250 km from the continent, the volcanic island of São Tomé has been colonized mostly by natural means, probably by the wind, since the emergence of the island about 15 million years ago, and presumably also by anthropogenic transportation of invasive and domestic species. To date, 37 different Drosophilid species have been mentioned from São Tomé. The present work extends this list to 80 species. The genera Zygothrica, Phorticella and Hypselothyrea are newly recorded from the island. Among these 80 species, only 12 are putatively introduced by human activities, suggesting the preponderance of natural arrivals. Compared to other islands, São Tomé harbours a high diversity of drosophilids. At least 14 species are supposed to be endemic. Future molecular comparisons between the island flies and their continental relatives will probably help to identify other endemic species. The high diversity observed in São Tomé is certainly due to the large size of the island, and to the presence of vast natural altitudinal forests offering a variety of possible habitats. Further collections are likely to lead to an increase of the species list. From now, São Tomé island appears as an excellent laboratory for studying the ecology and evolution of the Drosophila model.; La faune de Drosophilidae a été moins étudiée dans les îles afrotropicales de l’Atlantique que dans l’océan Indien. Située à environ 250 km du continent, l’île volcanique de São Tomé a été colonisée principalement de façon naturelle, probablement à l’aide du vent, depuis l’émergence de l’île il y a environ 15 millions d’années, et par le transport supposé d’espèces domestiques et invasives par l’activité humaine. Jusqu’à présent, 37 espèces de Drosophilidae étaient mentionnées à São Tomé. Le présent travail accroît cette liste à 80 espèces. Les genres Zygothrica, Phorticella et Hypselothyrea sont nouvellement cités de l’île. Parmi ces 80 espèces, seulement 12 pourraient avoir été introduites par les activités humaines, révélant la prépondérance des colonisations naturelles. Comparée à d’autres îles, São Tomé abrite une plus grande diversité de drosophiles. Au moins 14 espèces sont supposées être endémiques. Il est probable que d’autres espèces endémiques seront identifiées lorsque les études moléculaires permettront de comparer les individus de São Tomé avec les espèces apparentées du continent africain. La diversité observée à São Tomé est certainement due à la grande taille de l’île et à la présence d’une vaste forêt d’altitude offrant une grande variété d’habitats. De futures collectes permettront d’accroître la liste d’espèces. L’île de São Tomé apparaît comme un excellent territoire pour l’étude de l’écologie et de l’évolution du modèle drosophile.

Insects produce a variety of adhesives for diverse functions such as locomotion, mating, and egg or pupal anchorage to substrates. Although they are important for the biology of organisms and potentially represent a great resource for developing new materials, insect adhesives have been little studied so far. Here, we examined the adhesive properties of the larval glue of

BackgroundAt the very end of the larval stage Drosophila expectorate a glue secreted by their salivary glands to attach themselves to a substrate while pupariating. The glue is a mixture of apparently unrelated proteins, some of which are highly glycosylated and possess internal repeats. Because species adhere to distinct substrates (i.e. leaves, wood, rotten fruits), glue genes are expected to evolve rapidly.ResultsWe used available genome sequences and PCR-sequencing of regions of interest to investigate the glue genes in 20Drosophilaspecies. We discovered a new gene in addition to the seven glue genes annotated inD. melanogaster.We also identified a phase 1 intron at a conserved position present in five of the eight glue genes ofD. melanogaster, suggesting a common origin for those glue genes. A slightly significant rate of gene turnover was inferred. Both the number of repeats and the repeat sequence were found to diverge rapidly, even between closely related species. We also detected high repeat number variation at the intrapopulation level inD. melanogaster.ConclusionMost conspicuous signs of accelerated evolution are found in the repeat regions of several glue genes.

IntroductionMale genitalia are thought to ensure transfer of sperm through direct physical contact with female during copulation. However, little attention has been given to their pre-copulatory role with respect to sexual selection and sexual conflict. Males of the fruitflyDrosophila pacheahave a pair of asymmetric external genital lobes, which are primary sexual structures and stabilize the copulatory complex of female and male genitalia. We wondered if genital lobes inD. pacheamay have a role before or at the onset of copulation, before genitalia contacts are made.ResultsWe tested this hypothesis with aD. pacheastock where males have variable lobe lengths. In 92 mate competition trials with a single female and two males, females preferentially engaged into a first copulation with males that had a longer left lobe and that displayed increased courtship vigor. In 53 additional trials with both males having partially amputated left lobes of different lengths, we observed a weaker and non-significant effect of left lobe length on copulation success. Courtship durations significantly increased with female age and when two males courted the female simultaneously, compared to trials with only one courting male. In addition, lobe length did not affect sperm transfer once copulation was established.ConclusionLeft lobe length affects the chance of a male to engage into copulation. The morphology of this primary sexual trait may affect reproductive success by mediating courtship signals or by facilitating the establishment of genital contacts at the onset of copulation.

International audience; Animal terminalia represent some of the most diverse and rapidly evolving structures in the animal kingdom, and for this reason have been a mainstay in the taxonomic description of species. The terminalia of Drosophila melanogaster, with its wide range of experimental tools, have recently become the focus of increased interest in the fields of development, evolution, and behavior. However, studies from different disciplines have often used discrepant terminologies for the same anatomical structures. Consequently, the terminology of genital parts has become a barrier to integrating results from different fields, rendering it difficult to determine what parts are being referenced. We formed a consortium of researchers studying the genitalia of D. melanogaster to help establish a set of naming conventions. Here, we present a detailed visual anatomy of male genital parts, including a list of synonymous terms, and suggest practices to avoid confusion when referring to anatomical parts in future studies. The goal of this effort is to facilitate interdisciplinary communication and help newcomers orient themselves within the exciting field of Drosophila genitalia. ARTICLE HISTORY

Animal terminalia represent some of the most diverse and rapidly evolving structures in the animal kingdom, and for this reason have been a mainstay in the taxonomic description of species. The terminalia of Drosophila melanogaster, with its wide range of experimental tools, have recently become the focus of increased interest in the fields of development, evolution, and behavior. However, studies from different disciplines have often used discrepant terminologies for the same anatomical structures. Consequently, the terminology of genital parts has become a barrier to integrating results from different fields, rendering it difficult to determine what parts are being referenced. We formed a consortium of researchers studying the genitalia of D. melanogaster to help establish a set of naming conventions. Here, we present a detailed visual anatomy of male genital parts, including a list of synonymous terms, and suggest practices to avoid confusion when referring to anatomical parts in future studies. The goal of this effort is to facilitate interdisciplinary communication and help newcomers orient themselves within the exciting field of Drosophila genitalia.

BackgroundMale genitals have repeatedly evolved left-right asymmetries, and the causes of such evolution remain unclear. TheDrosophila nannopteragroup contains four species, among which three exhibit left-right asymmetries of distinct genital organs. In the most studied species,Drosophila pachea, males display asymmetric genital lobes and they mate right-sided on top of the female. Copulation position of the other species is unknown.ResultsTo assess whether the evolution of genital asymmetry could be linked to the evolution of one-sided mating, we examined phallus morphology and copulation position inD. pacheaand closely related species. The phallus was found to be symmetric in all investigated species exceptD. pachea, which display an asymmetric phallus with a right-sided gonopore, andD. acanthoptera, which harbor an asymmetrically bent phallus. In all examined species, males were found to position themselves symmetrically on top of the female, except inD. pacheaandD. nannoptera, where males mated right-sided, in distinctive, species-specific positions. In addition, the copulation duration was found to be increased innannopteragroup species compared to closely related outgroup species.ConclusionOur study shows that gains, and possibly losses, of asymmetry in genital morphology and mating position have evolved repeatedly in thenannopteragroup. Current data does not allow us to conclude whether genital asymmetry has evolved in response to changes in mating position, or vice versa.

CRISPR gene drive has recently been proposed as a promising technology for population management, including in conservation genetics. The technique would consist in releasing genetically engineered individuals that are designed to rapidly propagate a desired mutation or transgene into wild populations. Potential applications in conservation biology include the control of invasive pest populations that threaten biodiversity (eradication and suppression drives), or the introduction of beneficial mutations in endangered populations (rescue drives). The propagation of a gene drive is affected by different factors that depend on the drive construct (e.g. its fitness effect and timing of expression) or on the target species (e.g. its mating system and population structure). We review potential applications of the different types of gene drives for conservation. We examine the challenges posed by the evolution of resistance to gene drives and review the various molecular and environmental risks associated with gene drives (e.g. propagation to non-target populations or species and unintended detrimental ecosystem impacts). We provide some guidelines for future gene drive research and discuss ethical, biosafety and regulation issues., Funding for this project was provided by the CeMEB LabEx/University of Montpellier to NOR, ANR-14-ACHN-0003 to FD, INRA to AE and DB, INRA-SPE (SUZUCTICID project) to NOR and AE and European Research Council (FP7/2007-2013 Grant Agreement no. 337579) to VCO.

One promising application of CRISPR/Cas9 is to create targeted mutations to introduce traits of interest into domesticated organisms. However, a major current limitation for crop and livestock improvement is to identify the precise genes and genetic changes that must be engineered to obtain traits of interest. Here, we discuss the advantages of bio-inspired genome editing, i.e. the engineered introduction of natural mutations that have already been associated with traits of interest in other lineages (breeds, populations or species). To obtain a landscape view of potential targets for genome editing, we used Gephebase (www.gephebase.org), a manually curated database compiling published data about the genes responsible for evolutionary and domesticated changes across eukaryotes, and examined the >1200 mutations that have been identified in the coding regions of more than 700 genes in animals, plants and yeasts. We observe that our genetic knowledge is relatively important for certain traits, such as xenobiotic resistance, and poor for others. We also note that protein-null alleles, often owing to nonsense and frameshift mutations, represent a large fraction of the known loci of domestication (42% of identified coding mutations), compared with intraspecific (27%) and interspecific evolution (11%). Although this trend may be subject to detection, publication and curation biases, it is consistent with the idea that breeders have selected large-effect mutations underlying adaptive traits in specific settings, but that these mutations and associated phenotypes would not survive the vagaries of changing external and internal environments. Our compilation of the loci of evolution and domestication uncovers interesting options for bio-inspired and transgene-free genome editing.

Gene drive has recently been proposed as a promising technology for population management, including in conservation genetics; it is based on the release of genetically engineered individuals designed to rapidly propagate a desired mutation or transgene to high frequencies in wild populations. Potential applications in conservation biology include the control of invasive pest populations that threaten biodiversity (eradication and suppression drives), or the introduction of beneficial mutations in endangered populations (rescue drives). We examine the challenges posed by the evolution of resistance to gene drives and review the various environmental risks associated with gene drives. Contrary to suppression and eradication drives, the evolution of resistance should not prevent the fixation of rescue drives, while countermeasures to stop their spread are likely to fail. For eradication and suppression drives, minimizing the chances of resistance evolution requires targeting genes whose sequences have low polymorphism in natural populations (e.g. that are functionally constrained), which might however increase the odds of gene drive propagation to non-target populations/species. Conversely, targeting sequences that are present in the target population/species, but absent in non-target populations/species, might increase the odds of resistance evolution due to the introgression of resistant alleles from non-target populations/species. Once a gene drive has fixed in a target population, the time it persists before being inactivated by mutations influences its risk of spread to non-target populations/species. Finally, ethical values along with a clear regulatory framework for risk assessment should guide gene drive research.

Diverse traits often covary between species [1-3]. The possibility that a single mutation could contribute to the evolution of several characters between species [3] is rarely investigated as relatively few cases are dissected at the nucleotide level. Drosophila santomea has evolved additional sex comb sensory teeth on its legs and has lost two sensory bristles on its genitalia. We present evidence that a single nucleotide substitution in an enhancer of the scute gene contributes to both changes. The mutation alters a binding site for the Hox protein Abdominal-B in the developing genitalia, leading to bristle loss, and for another factor in the developing leg, leading to bristle gain. Our study suggests that morphological evolution between species can occur through a single nucleotide change affecting several sexually dimorphic traits. VIDEO ABSTRACT.

Diverse traits often covary between species. The possibility that a single mutation could contribute to the evolution of several characters between species is rarely investigated as relatively few cases are dissected at the nucleotide level. Drosophila santomea has evolved additional sex comb sensory teeth on its legs and has lost two sensory bristles on its genitalia. We found that a single nucleotide substitution in an enhancer of the scute gene contributes to both changes. The mutation alters a binding site for the Hox protein Abdominal-B in the developing genitalia, leading to bristle loss, and for another factor in the developing leg, leading to bristle gain. Our study shows that morphological evolution between species can occur through a single nucleotide change affecting several sexually dimorphic traits.

Repetitions in the mutations found to be responsible for independent evolution of similar phenotypes in various taxa have led some biologists to propose that for certain evolutionary changes the causal mutations are predictable. We examine here the nature of the predictions that have been made and their associated arguments. Predictions about the loci of past evolution are retrodictions, i.e. inferences about events that occurred in the past. They are not based on elaborate models and they derive mainly from the observation of repeated cases of genetic evolution. Predictions at the nucleotide level or at the gene level have a higher inference gain than those for broader categories of genetic changes such as cis-regulatory mutations.

Background Multiple animal species exhibit morphological asymmetries in male genitalia. In insects, left-right genital asymmetries evolved many times independently and have been proposed to appear in response to changes in mating position. However, little is known about the relationship between mating position and the interaction of male and female genitalia during mating, and functional analyses of asymmetric morphologies in genitalia are virtually non-existent. We investigated the relationship between mating position, asymmetric genital morphology and genital coupling in the fruit fly Drosophila pachea, in which males possess an asymmetric pair of external genital lobes and mate in an unusual right-sided position on top of the female. Results We examined D. pachea copulation by video recording and by scanning electron microscopy of genital complexes. We observed that the interlocking of male and female genital organs in D. pachea is remarkably different from genital coupling in the well-studied D. melanogaster. In D. pachea, the female oviscapt valves are asymmetrically twisted during copulation. The male’s asymmetric lobes tightly grasp the female’s abdomen in an asymmetric ‘locking’ position, with the left and right lobes contacting different female structures. The male anal plates, which grasp the female genitalia in D. melanogaster, do not contact the female in D. pachea. Experimental lobe amputation by micro-surgery and laser-ablation of lobe bristles led to aberrant coupling of genitalia and variable mating positions, in which the male was tilted towards the right side of the female. Conclusion We describe, for the first time, how the mating position depends on coupling of male and female genitalia in a species with asymmetric genitalia and one-sided mating position. Our results show that D. pachea asymmetric epandrial lobes do not act as a compensatory mechanism for the change from symmetric to one-sided mating position that occurred during evolution of D. pachea’s ancestors, but as holding devices with distinct specialized functions on the left and right sides. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0747-4) contains supplementary material, which is available to authorized users.