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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. ​

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.

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.

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.

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.

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

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.

Rearing temperature is correlated with the timing and speed of development in a wide range of poikiloterm animals that do not regulate their body temperature. However, exceptions exist, especially in species that live in environments with high temperature extremes or oscillations. Drosophila pachea is endemic to the Sonoran desert in Mexico, in which temperatures and temperature variations are extreme. We wondered if the developmental timing in D. pachea may be sensitive to differing rearing temperatures or if it remains constant. We determined the overall timing of the Drosophila pachea life-cycle at 25{degrees}C and 29{degrees}C. The duration of pupal development was similar at both temperatures although the relative progress differed at particular stages. Thus, D. pachea may have evolved mechanisms to buffer temperature influence on developmental speed, potentially to ensure proper development and individuals fitness in desert climate conditions. HighlightsO_LIIn poikilotherms, developmental speed usually increases with rearing temperature C_LIO_LIGlobal pupal development of D. pachea is similar at two different rearing temperatures C_LIO_LIDiscrete temperature dependent timing differences at specific pupal stages C_LIO_LID. pachea development is longer compared to other Drosophila species C_LIO_LITemperature-buffering mechanisms may have evolved to ensure a proper development C_LI