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The loss of discrete morphological traits, the most common evolutionary transition, is typically driven by changes in developmental gene expression. Mutations accumulating in regulatory elements of these genes can disrupt DNA binding sites for transcription factors patterning their spatial expression, or delete entire enhancers. Regulatory elements, however, may be silenced through changes in chromatin accessibility or the emergence of repressive elements. Here, we show that increased chromatin accessibility at the gene yellow , combined with the gain of a repressor site, underlies the loss of a wing spot pigmentation pattern in a Drosophila species. The gain of accessibility of this repressive element is regulated by E93, a transcription factor governing the progress of metamorphosis. This convoluted evolutionary scenario contrasts with the parsimonious mutational paths generally envisioned and often documented for morphological losses. It illustrates how evolutionary changes in chromatin accessibility may directly contribute to morphological diversification.

Colonization of a novel ecological niche can require, or be driven by, evolution of an animal’s behaviors promoting their reproductive success in the new environment. Little is known about the underlying mechanisms. We have exploited an emerging genetic model for behavioral neuroecology, Drosophila sechellia – a close relative of Drosophila melanogaster that exhibits extreme specialism for Morinda citrifolia noni fruit – to study the evolution and sensory basis of oviposition. D. sechellia produces fewer eggs compared to other drosophilids, but lays these almost exclusively on noni substrates, contrasting with avoidance or indifference of noni by generalist species. Visual, textural and social cues do not explain the species-specificity of this preference. By contrast, loss of olfactory input in D. sechellia, but not D. melanogaster, essentially abolishes egg-laying, suggesting that this sensory modality gates gustatory-driven noni preference. We find the noni bouquet is detected by redundant olfactory pathways. By parsing the fruit’s volatile chemicals and genetic perturbation of individual olfactory pathways in D. sechellia, we discover a key role for hexanoic acid and its cognate receptor, the Ionotropic receptor Ir75b, in odor-evoked oviposition. Through receptor exchange in D. melanogaster, we provide evidence for a causal contribution of odor-tuning changes in Ir75b to the evolution of oviposition behavior during D. sechellia’s host specialization.

The species of Syzeton Blackburn, 1891 (=Zonantes Casey, 1895, syn. nov.) known from the United States are revised. All species formerly placed under Zonantes Casey, 1895 are transferred to Syzeton Blackburn, 1891: S. ouachitanus (Werner, 1990), comb. nov.; S. fasciatus (Melsheimer, 1846), comb. nov.; S. hubbardi (Casey, 1895), comb. nov.; S. nubifer (LeConte, 1878), comb. nov.; S. ater (LeConte, 1875), comb. nov.; S. pallidus (Werner, 1990), comb. nov.; S. subfasciatus (LeConte, 1875), comb. nov.; S. floridanus (Werner, 1990), comb. nov.; S. signatus (Haldeman, 1848), comb. nov.). Additionally, three new species are described herein: Syzeton gruberi n. sp., Syzeton arizonae n. sp., both from Arizona, and Syzeton belovi n. sp., from Texas, Oklahoma and Florida. Finally, Zonantes mississippiensis Werner, 1990 is considered a junior synonym of Syzeton ouachitanus (Werner, 1990), syn. nov.

The gene regulatory network governing anterior–posterior axis formation in Drosophila is a well-established paradigm to study transcription in developmental biology. The rapid temporal dynamics of gene expression during early stages of development, however, are difficult to track with standard techniques. We optimized the bright and fast-maturing fluorescent protein mNeonGreen as a real-time, quantitative reporter of enhancer expression. We derive enhancer activity from the reporter fluorescence dynamics with high spatial and temporal resolution, using a robust reconstruction algorithm. By comparing our results with data obtained with the established MS2-MCP system, we demonstrate the higher detection sensitivity of our reporter. We used the reporter to quantify the activity of variants of a simple synthetic enhancer, and observe increased activity upon reduction of enhancer–promoter distance or addition of binding sites for the pioneer transcription factor Zelda. Our reporter system constitutes a powerful tool to study spatio-temporal gene expression dynamics in live embryos., Ceolin et al. optimise the fluorescent protein mNeonGreen to generate a reporter to measure enhancer expression in living Drosophila embryos. They also find that reduced enhancer–promoter distance or addition of binding sites for the pioneer transcription factor Zelda increases enhancer activity.

The diversity of forms in multicellular organisms originates largely from the spatial redeployment of developmental genes [S. B. Carroll, Cell 134, 25-36 (2008)]. Several scenarios can explain the emergence of cis-regulatory elements that govern novel aspects of a gene expression pattern [M. Rebeiz, M. Tsiantis, Curr. Opin. Genet. Dev. 45, 115-123 (2017)]. One scenario, enhancer co-option, holds that a DNA sequence producing an ancestral regulatory activity also becomes the template for a new regulatory activity, sharing regulatory information. While enhancer co-option might fuel morphological diversification, it has rarely been documented [W. J. Glassford et al., Dev. Cell 34, 520-531 (2015)]. Moreover, if two regulatory activities are borne from the same sequence, their modularity, considered a defining feature of enhancers [J. Banerji, L. Olson, W. Schaffner, Cell 33, 729-740 (1983)], might be affected by pleiotropy. Sequence overlap may thereby play a determinant role in enhancer function and evolution. Here, we investigated this problem with two regulatory activities of the Drosophila gene yellow, the novel spot enhancer and the ancestral wing blade enhancer. We used precise and comprehensive quantification of each activity in Drosophila wings to systematically map their sequences along the locus. We show that the spot enhancer has co-opted the sequences of the wing blade enhancer. We also identified a pleiotropic site necessary for DNA accessibility of a shared regulatory region. While the evolutionary steps leading to the derived activity are still unknown, such pleiotropy suggests that enhancer accessibility could be one of the molecular mechanisms seeding evolutionary co-option.

Summary A recent study identifies the neuronal and molecular underpinnings of a key ecological difference between two Drosophila species using a remarkable genetic toolbox for a non-model species.

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.

Establishment of spatial coordinates during Drosophila embryogenesis relies on differential regulatory activity of axis patterning enhancers. Concentration gradients of activator and repressor transcription factors (TFs) provide positional information to each enhancer, which in turn promotes transcription of a target gene in a specific spatial pattern. However, the interplay between an enhancer regulatory activity and its accessibility as determined by local chromatin organization is not well understood. We profiled chromatin accessibility with ATAC-seq in narrow, genetically tagged domains along the antero-posterior axis in the Drosophila blastoderm. We demonstrate that one-quarter of the accessible genome displays significant regional variation in its ATAC-seq signal immediately after zygotic genome activation. Axis patterning enhancers are enriched among the most variable intervals, and their accessibility changes correlate with their regulatory activity. In an embryonic domain where an enhancer receives a net activating TF input and promotes transcription, it displays elevated accessibility in comparison to a domain where it receives a net repressive input. We propose that differential accessibility is a signature of patterning cis-regulatory elements in the Drosophila blastoderm and discuss potential mechanisms by which accessibility of enhancers may be modulated by activator and repressor TFs.

Following a previous revision of species of the genus Mixaderus Collado & Alonso-Zarazaga, 1996 (Coleoptera: Aderidae) from Madagascar and the Mascarene islands, I describe here six new species from the same genus from La Réunion and Mauritius: Mixaderus reunionensis n. sp.; Mixaderus chassaini n. sp.; Mixaderus lemagneni n. sp.; Mixaderus tamisieri n. sp.; Mixaderus voisini n. sp.; Mixaderus mauritiensis n. sp. I also provide an updated key to the Mixaderus species from the Mascarene archipelago.

The Aderidae (Coleoptera: Tenebrionoidea) of Cabo Verde (or Cape Verde in English transcription) Archipelago in the Central Atlantic Ocean is revised based on an examination of types and additional material. Four species are confirmed for the archipelago, three of the genus Cobososia Collado et Alonso-Zarazaga, 1996 and one of the genus Aderus Stephens, 1829. We also propose to transfer Anthicus reductus Wollaston, 1867 (Anthicidae: Anthicinae: Anthicini) to the genus Cobososia (Aderidae), as Cobososia reducta (Wollaston, 1867) comb. nov. and demonstrate, that Cobososia angulithorax (Desbrochers des Loges, 1881) is conspecific with Cobososia reducta (Wollaston, 1867) syn. nov. Finally, we present new records and an illustrated identification key to the ant-like leaf beetles of Cabo Verde.

The genitalia present some of the most rapidly evolving anatomical structures in the animal kingdom, possessing a variety of parts that can distinguish recently diverged species. In the Drosophila melanogaster group, the phallus is adorned with several processes, pointed outgrowths, that are similar in size and shape between species. However, the complex three-dimensional nature of the phallus can obscure the exact connection points of each process. Previous descriptions based upon adult morphology have primarily assigned phallic processes by their approximate positions in the phallus and have remained largely agnostic regarding their homology relationships. In the absence of clearly identified homology, it can be challenging to model when each structure first evolved. Here, we employ a comparative developmental analysis of these processes in eight members of the melanogaster species group to precisely identify the tissue from which each process forms. Our results indicate that adult phallic processes arise from three pupal primordia in all species. We found that in some cases the same primordia generate homologous structures whereas in other cases, different primordia produce phenotypically similar but remarkably non-homologous structures. This suggests that the same gene regulatory network may have been redeployed to different primordia to induce phenotypically similar traits. Our results highlight how traits diversify and can be redeployed, even at short evolutionary scales.Research HighlightBy incorporating developmental analysis, we find that genital structures previously identified as homologs are novel structures. This highlights how developmental analysis can help resolve contentious claims of homology.

A high density of regulatory information encodes a quantitative spatial pattern in a Drosophila transcriptional enhancer., Developmental enhancers control the expression of genes prefiguring morphological patterns. The activity of an enhancer varies among cells of a tissue, but collectively, expression levels in individual cells constitute a spatial pattern of gene expression. How the spatial and quantitative regulatory information is encoded in an enhancer sequence is elusive. To link spatial pattern and activity levels of an enhancer, we used systematic mutations of the yellow spot enhancer, active in developing Drosophila wings, and tested their effect in a reporter assay. Moreover, we developed an analytic framework based on the comprehensive quantification of spatial reporter activity. We show that the quantitative enhancer activity results from densely packed regulatory information along the sequence, and that a complex interplay between activators and multiple tiers of repressors carves the spatial pattern. Our results shed light on how an enhancer reads and integrates trans-regulatory landscape information to encode a spatial quantitative pattern.

This work represents a provisional inventory of Asian species placed in the genus Zarcosia Collado & Alonso-Zarazaga, 1996. Most of these species had not been reassigned since their original description under now obsolete genera, in spite of the morphological homogeneity of the genus Zarcosia Collado & Alonso-Zarazaga, 1996. The present work includes the following transfers resulting in 34 new combinations: Z. armipes (Fairmaire, 1896), comb. nov.; Z. batuensis (Werner, 1962), comb. nov.; Z. bipartita (Pic, 1901), comb. nov.; Z. capitalis (Pic, 1901), comb. nov.; Z. cephalica (Werner, 1962), comb. nov.; Z. dentatifemur (Pic, 1912), comb. nov.; Z. discoidalis (Pic, 1902), comb. nov.; Z. genjiensis (Pic, 1917), comb. nov.; Z. glaucescens (Champion, 1920), comb. nov.; Z. grandiceps (Pic, 1899), comb. nov.; Z. holosericea (Champion, 1916), comb. nov.; Z. javana (Pic, 1894), comb. nov.; Z. kempi (Blair, 1924), comb. nov.; Z. longithorax (Pic, 1899), comb. nov.; Z. lucifuga (Heberdey, 1931), comb. nov.; Z. luteitarsis (Champion, 1924), comb. nov.; Z. malayana (Werner, 1962), comb. nov.; Zarcosia nathani (Pic, 1943), comb. nov.; Z. nigrofasciata (Pic, 1899), comb. nov.; Z. obscuricornis (Pic, 1927), comb. nov.; Z. palliditarsis (Pic, 1912), comb. nov.; Z. patucki (Champion, 1924), comb. nov.; Z. picina (Fairmaire, 1893), comb. nov.; Z. plumbea (Champion, 1916), comb. nov.; Z. proprior (Pic, 1920), comb. nov.; Z. rubrobasalis (Pic, 1921), comb. nov.; Z. rufotestacea (Pic, 1901), comb. nov.; Z. sellata (Champion, 1916), comb. nov.; Z. sexdentata (Champion, 1924), comb. nov.; Z. subrobusta (Pic, 1943), comb. nov.; Z. subrufa (Champion, 1924), comb. nov.; Z. testaceitarsis (Pic, 1926), comb. nov.; Z. troglodytes (Champion, 1916), comb. nov.; Z. uncifer (Champion, 1916), comb. nov. In addition, based on the study of over 200 Asian specimens, the geographical distribution of each species is outlined. The study of numerous collections lead me to recognize 14 new species, distinguishable, at least by male genitalia, that I describe here: Zarcosia barlayi n. sp., Zarcosia bedosae n. sp., Zarcosia brunnea n. sp., Zarcosia deharvengi n. sp., Zarcosia gerstmeieri n. sp., Zarcosia ilonae n. sp., Zarcosia intermedia n. sp., Zarcosia lemairei n. sp., Zarcosia schawalleri n. sp., Zarcosia sinuata n. sp., Zarcosia spinifemur n. sp. Zarcosia srilankaensis n. sp., Zarcosia sumatrensis n. sp. and Zarcosia weigeli n. sp. Finally, I propose a new synonymy for Hylophilus picinus var. rufescens Pic, 1905 = Zarcosia picina (Fairmaire, 1893), syn. nov. and design two lectotypes, for Xylophilus picinus, Fairmaire, 1893, pres. design. and for Zarcosia subglaber Pic, 1952 pres. design.

The diversity of forms in multicellular organisms originates largely from the spatial redeployment of developmental genes [S. B. Carroll

Transcriptional enhancers are short DNA sequences controlling the spatial activity, timing and levels of eukaryotic gene transcription. Their quantitative transcriptional output is thought to result from the number and organization of transcription factor binding sites (TFBSs). Yet, how the various aspects of regulatory information are encoded in enhancer sequences remains elusive. We addressed this question by quantifying the spatial activity of theyellow spotenhancer active in developingDrosophilawings. To identify which enhancer DNA sequence contributes to enhancer activity, we introduced systematic mutations along the enhancer. We developed an analytic framework that uses comprehensive descriptors to quantify reporter assay in transgenic flies and measure spatial variations in activity levels across the wing. Our analysis highlights an unexpected density of regulatory information in thespotenhancer sequence. Furthermore, it reveals an unanticipated regulatory logic underlying the activity of this enhancer, and how it reads the wingtrans-regulatory landscape to encode a spatial pattern.

Over the past decade, the spotted wing Drosophila, Drosophila suzukii, has invaded Europe and America and has become a major agricultural pest in these areas, thereby prompting intense research activities to better understand its biology. Two draft genome assemblies based on short-read sequencing were released in 2013 for this species. Although valuable, these resources contain pervasive assembly errors and are highly fragmented, two features limiting their values. Our purpose here was to improve the assembly of the D. suzukii genome. For this, we generated PacBio long-read sequencing data at 160X sequence coverage and assembled a novel, contiguous D. suzukii genome. We obtained a high-quality assembly of 270 Mb (with 546 contigs, a N50 of 2.6Mb, a L50 of 15, and a BUSCO score of 95%) that we called WT3-2.0. We found that despite 16 rounds of full-sib crossings the D. suzukii strain that we sequenced has maintained high levels of polymorphism in some regions of its genome (ca. 19Mb). As a consequence, the quality of the assembly of these regions was reduced. We explored possible origins of this high residual diversity, including the presence of structural variants and a possible heterogeneous admixture pattern of North American and Asian ancestry. Overall, our WT3-2.0 assembly provides a higher quality genomic resource compared to the previous one in terms of general assembly statistics, sequence quality and gene annotation. This new D. suzukii genome assembly is therefore an improved resource for high-throughput sequencing approaches, as well as manipulative genetic technologies to study D. suzukii.

The males of two closely related species of fly respond differently to a female pheromone. It emerges that this difference is due to alterations in the activity of an evolutionarily conserved neural circuit in the brain. The males of two closely related species of fly respond differently to a female pheromone. It emerges that this difference is due to alterations in the activity of an evolutionarily conserved neural circuit in the brain.

Hox genes pattern the anterior-posterior axis of animals, and are posited to drive animal body plan evolution, yet their precise role in evolution has been difficult to determine. Here, we identified evolutionary modifications in the Hox gene Abd-B that dramatically altered its expression along the body plan of Drosophila santomea. Abd-B is required for pigmentation in Drosophila yakuba, the sister species of D. santomea, and changes to Abd-B expression would be predicted to make large contributions to the loss of body pigmentation in D. santomea. However, manipulating Abd-B expression in current-day D. santomea does not affect pigmentation. We attribute this epistatic interaction to four other genes within the D. santomea pigmentation network, three of which have evolved expression patterns that do not respond to Abd-B. Our results demonstrate how body plans may evolve through small evolutionary steps distributed throughout Hox regulated networks. Polygenicity and epistasis may hinder efforts to identify genes and mechanisms underlying macroevolutionary traits.

International audience; Egg-laying behavior is one of the most important aspects of female behavior, and has a profound impact on the fitness of a species. As such, it is controlled by several layers of regulation. Here, we review recent advances in our understanding of insect neural circuits that control when, where and how to lay an egg. We also outline outstanding open questions about the control of egg-laying decisions, and speculate on the possible neural underpinnings that can drive the diversification of oviposition behaviors through evolution.

During the past decade, Drosophila suzukii has established itself as a global invasive fruit pest, enabled by its ability to lay eggs into fresh, ripening fruit. In a previous study, we investigated the impact of different strawberry accessions on the development of D. suzukii eggs, in the search of natural resistance. We identified several accessions that significantly reduced adult fly emergence from infested fruit. In the present study, we aimed at understanding the chemical basis of this effect. We first noted that one of the more resistant accessions showed an unusual enrichment of methyl anthranilate within its fruit, prompting us to investigate this fruit compound as a possible cause limiting fly development. We found that methyl anthranilate alone triggers embryo lethality in a concentration-dependent manner, unlike another comparable organic fruit compound. We also showed that a chemical fraction of the resistant strawberry accession that contains methyl anthranilate carries some activity toward the egg hatching rate. Surprisingly, in spite of the lethal effect of this compound to their eggs, adult females are not only attracted to methyl anthranilate at certain concentrations, but they also display a concentration-dependent preference to lay on substrates enriched in methyl anthranilate. This study demonstrates that methyl anthranilate is a potent agonist molecule against D. suzukii egg development. Its elevated concentration in a specific strawberry accession proven to reduce the fly development may explain, at least in part the fruit resistance. It further illustrates how a single, natural compound, non-toxic to humans could be exploited for biological control of a pest species.

Measurements of open chromatin in specific cell types are widely used to infer the spatiotemporal activity of transcriptional enhancers. How reliable are these predictions? In this review, it is argued that the relationship between the accessibility and activity of an enhancer is insufficiently described by simply considering open versus closed chromatin, or active versus inactive enhancers. Instead, recent studies focusing on the quantitative nature of accessibility signal reveal subtle differences between active enhancers and their different inactive counterparts: the closed silenced state and the accessible primed and repressed states. While the open structure as such is not a specific indicator of enhancer activity, active enhancers display a higher degree of accessibility than the primed and repressed states. Molecular mechanisms that may account for these quantitative differences are discussed. A model that relates molecular events at an enhancer to changes in its activity and accessibility in a developing tissue is also proposed.

Morphological diversity is dominated by variation in body proportion. Yet the cellular processes underlying differential growth of morphological traits between species remain largely unknown. Here we compare the ovipositors of two closely related species,Drosophila melanogasterandD. suzukii.D. suzukiihas switched its egg-laying niche from rotting to ripe fruit. Along with this shift, theD. suzukiiovipositor has undergone a significant change in size and shape. Using an allometric approach we find that, while adult ovipositor width has hardly changed between the species,D. suzukiiovipositor length is almost double that ofD. melanogaster. We show that this size difference mostly arises during a 6-hour time window in the middle of pupal development. We observe that the developing ovipositors of the two species comprise an almost identical number of cells, with a very similar profile of cell shapes and orientations. After cell division stops, we find that the ovipositor area continues to grow through the isotropic expansion of cell apical area. Remarkably, at one point, the rate of cell apical area expansion is more than 4 times faster inD. suzukiithan inD. melanogaster. In addition, we find that an anisotropic cellular reorganization of the developing ovipositor results in a net elongation of the tissue, despite the isotropic expansion of cell size, and is enhanced inD. suzukii. Therefore, the quantitative fine-tuning of shared, morphogenetic processes -the rate of cell size expansion and the cellular rearrangements–can drive macroscopic evolutionary changes in organ size and shape.

Establishment of spatial coordinates during Drosophila embryogenesis relies on differential regulatory activity of axis patterning enhancers. Concentration gradients of activator and repressor transcription factors (TFs) provide positional information to each enhancer, which in turn promotes transcription of a target gene in a specific spatial pattern. However, the interplay between an enhancer regulatory activity and its accessibility as determined by local chromatin organization is not well understood. We profiled chromatin accessibility with ATAC-seq in narrow, genetically tagged domains along the antero-posterior axis in the Drosophila blastoderm. We demonstrate that one-quarter of the accessible genome displays significant regional variation in its ATAC-seq signal immediately after zygotic genome activation. Axis patterning enhancers are enriched among the most variable intervals, and their accessibility changes correlate with their regulatory activity. In an embryonic domain where an enhancer receives a net activating TF input and promotes transcription, it displays elevated accessibility in comparison to a domain where it receives a net repressive input. We propose that differential accessibility is a signature of patterning cis-regulatory elements in the Drosophila blastoderm and discuss potential mechanisms by which accessibility of enhancers may be modulated by activator and repressor TFs.

Gompel, Nicolas, Kopp, Artyom (2018): Drosophila (Sophophora) carrolli n. sp., a new species from Brunei, closely related to Drosophila (Sophophora) rhopaloa Bock & Wheeler, 1972 (Diptera: Drosophilidae). Zootaxa 4434 (3): 502-510, DOI: https://doi.org/10.11646/zootaxa.4434.3.6

International audience; Pigmentation is a diverse and ecologically relevant trait in insects. Pigment formation has been studied extensively at the genetic and biochemical levels. The temporality of pigment formation during animal development, however, is more elusive. Here, we examine this temporality, focusing on yellow, a gene involved in the formation of black melanin. We generated a protein-tagged yellow allele in the fruit fly Drosophila melanogaster, which allowed us to precisely describe Yellow expression pattern at the tissue and cellular levels throughout development. We found Yellow expressed in the pupal epidermis in patterns prefiguring black pigmentation. We also found Yellow expressed in a few central neurons from the second larval instar to adult stages, including a subset of neurons adjacent to the clock neurons marked by the gene Pdf. We then specifically examined the dynamics of Yellow expression domain and subcellular localization in relationship to pigment formation. In particular, we showed how a late step of re-internalization is regulated by the large low-density lipoprotein receptor-related protein Megalin. Finally we suggest a new function for Yellow in the establishment of sharp pigmentation pattern boundaries, whereby this protein may assume a structural role, anchoring pigment deposits or pigmentation enzymes in the cuticle.

This work provides a taxonomic survey of the North American species of the genus Elonus Casey, 1895 (Coleoptera: Tenebrionoidea: Aderidae). It includes the description of a new species, Elonus gruberi n. sp. from the United States, related to E. hesperus Werner, 1990 and to E. basalis (LeConte, 1855). A review and key to the North American species is provided.

Patterns of stripes on bird plumage are determined from deep under the skin

Summary Morphological diversity is dominated by variation in body proportion [1], which can be described with scaling relationships and mathematical equations, following the pioneering work of D’Arcy Thompson [2] and Julian Huxley [3]. Yet, the cellular processes underlying divergence in size and shape of morphological traits between species remain largely unknown [4, 5, 6, 7, 8]. Here, we compare the ovipositors of two related species, Drosophila melanogaster and D. suzukii. D. suzukii has switched its egg-laying niche from rotting to ripe fruit [9]. Along with this shift, the D. suzukii ovipositor has undergone a significant change in size and shape [10]. Using an allometric approach, we find that, while adult ovipositor width has hardly changed between the species, D. suzukii ovipositor length is almost double that of D. melanogaster. We show that this difference mostly arises in a 6-h time window during pupal development. We observe that the developing ovipositors of the two species comprise an almost identical number of cells, with a similar profile of cell shapes and orientations. After cell division stops, we find that the ovipositor area continues to grow in both species through the isotropic expansion of cell apical area and the anisotropic cellular reorganization of the tissue. Remarkably, we find that the lengthening of the D. suzukii ovipositor compared to that of D. melanogaster results from the combination of the accelerated expansion of apical cell size and the enhanced anisotropic rearrangement of cells in the tissue. Therefore, the quantitative fine-tuning of morphogenetic processes can drive evolutionary changes in organ size and shape., Graphical Abstract, Highlights • D. suzukii has evolved a bigger egg-laying organ compared to D. melanogaster • The inter-species size difference arises during a short development time window • The fine-tuning of shared cellular processes drives this difference in morphogenesis • The rate of cell apical area expansion and the tissue shape anisotropy have evolved, The fruit pest species Drosophila suzukii has evolved a bigger egg-laying organ compared to D. melanogaster. Green et al. show that the fine-tuning of shared cellular processes—namely, the rate of cell apical area expansion and the tissue shape anisotropy—drives the change in size and shape of the egg-laying organ of D. suzukii.

Drosophila suzukii is threatening soft fruit production worldwide due to the females’ ability to pierce through the intact skin of ripe fruits and lay eggs inside. Larval consumption and the associated microbial infection cause rapid fruit degradation, thus drastic yield and economic loss. Cultivars that limit the proliferation of flies may be ideal to counter this pest; however they have not yet been developed or identified. To search for potential breeding material, we investigated the rate of adult D. suzukii emergence from individual fruits (fly emergence) of 107 accessions of Fragaria species that had been exposed to egg-laying D. suzukii females. We found significant variation in fly emergence across accessions, which correlated with the genetic make-up of the accessions and fruit diameter, and to a lesser extent with the strawberry species background. We identified accessions with significant resistance to fly emergence, not related to their fruit diameter. These accessions constitute valuable breeding material for strawberry cultivars that limit D. suzukii spread.

The ability to find and consume nutrient-rich diets for successful reproduction and survival is fundamental to animal life. Among the nutrients important for all animals are polyamines, a class of pungent smelling compounds required in numerous cellular and organismic processes. Polyamine deficiency or excess has detrimental effects on health, cognitive function, reproduction, and lifespan. Here, we show that a diet high in polyamine is beneficial and increases reproductive success of flies, and we unravel the sensory mechanisms that attract Drosophila to polyamine-rich food and egg-laying substrates. Using a combination of behavioral genetics and in vivo calcium imaging, we demonstrate that Drosophila uses multisensory detection to find and evaluate polyamines present in overripe and fermenting fruit, their favored feeding and egg-laying substrate. In the olfactory system, two coexpressed ionotropic receptors (IRs), IR76b and IR41a, mediate the long-range attraction to the odor. In the gustatory system, multimodal taste sensation by IR76b receptor and GR66a bitter receptor neurons is used to evaluate quality and valence of the polyamine providing a mechanism for the fly's high attraction to polyamine-rich and sweet decaying fruit. Given their universal and highly conserved biological roles, we propose that the ability to evaluate food for polyamine content may impact health and reproductive success also of other animals including humans.

The independent evolution of morphological similarities is widespread. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common. However, for more complex traits, the possible genetic paths may be more numerous; the molecular mechanisms underlying their independent origins and the extent to which they are constrained to follow certain genetic paths are largely unknown. Here we show that a male wing pigmentation pattern involved in courtship display has been gained and lost multiple times in a Drosophila clade. Each of the cases we have analysed (two gains and two losses) involved regulatory changes at the pleiotropic pigmentation gene yellow. Losses involved the parallel inactivation of the same cis-regulatory element (CRE), with changes at a few nucleotides sufficient to account for the functional divergence of one element between two sibling species. Surprisingly, two independent gains of wing spots resulted from the co-option of distinct ancestral CREs. These results demonstrate how the functional diversification of the modular CREs of pleiotropic genes contributes to evolutionary novelty and the independent evolution of morphological similarities.

The gain, loss or modification of morphological traits is generally associated with changes in gene regulation during development. However, the molecular bases underlying these evolutionary changes have remained elusive. Here we identify one of the molecular mechanisms that contributes to the evolutionary gain of a male-specific wing pigmentation spot in Drosophila biarmipes, a species closely related to Drosophila melanogaster. We show that the evolution of this spot involved modifications of an ancestral cis-regulatory element of the yellow pigmentation gene. This element has gained multiple binding sites for transcription factors that are deeply conserved components of the regulatory landscape controlling wing development, including the selector protein Engrailed. The evolutionary stability of components of regulatory landscapes, which can be co-opted by chance mutations in cis-regulatory elements, might explain the repeated evolution of similar morphological patterns, such as wing pigmentation patterns in flies.

The lateral line of the zebrafish has many of the advantages that made the sensory organs of Drosophila a very productive model system: 1) it comprises a set of discrete sense organs (neuromasts) arranged in a defined, species-specific pattern, such that each organ can be individually recognized; 2) the neuromasts are superficial and easy to visualize, and the innervating neurons are easy to label; 3) the sensory projection is simple yet reproducibly organized. Here we describe some of the tools that can be used to investigate the development of this system, and we illustrate their usefulness with specific examples. We conclude that the lateral line is uniquely suited among vertebrate sensory systems for a molecular, cellular and genetic analysis of pattern formation and of neural development.

Some morphological traits differ greatly between related species, but it is not clear whether diversity evolves through changes in the same genes and whether similar, independent (that is, convergent) changes occur by the same mechanism1,2. Pigmentation in fruitflies presents an attractive opportunity to explore these issues because pigmentation patterns are diverse, similar patterns have arisen in independent clades, and numerous genes governing their formation have been identified3,4,5 in Drosophila melanogaster. Here we show that both evolutionary diversification and convergence can be due to evolution at the same locus, by comparing abdominal pigmentation and trichome patterns and the expression of Bric-a-brac2 (Bab2), which regulates both traits in D. melanogaster3,6, in 13 species representing the major clades7,8 of the subfamily Drosophilinae. Modifications of Bab2 expression are frequently correlated with diverse pigmentation and trichome patterns that evolved independently in multiple lineages. In a few species, Bab2 expression is not correlated with changes in pigmentation but is correlated with a conserved pattern of trichomes, indicating that this locus can be circumvented to evolve new patterns when a correlated trait is under different constraints.

The lateral line of fish and amphibians is a sensory system that comprises a number of individual sense organs, the neuromasts, arranged in a defined pattern on the surface of the body. A conspicuous part of the system is a line of organs that extends along each flank (and which gave the system its name). At the end of zebrafish embryogenesis, this line comprises 7-8 neuromasts regularly spaced between the ear and the tip of the tail. The neuromasts are deposited by a migrating primordium that originates from the otic region. Here, we follow the development of this pattern and show that heterogeneities within the migrating primordium prefigure neuromast formation.