Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit.
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ABSTRACT:
SUBMITTER: Keesey IW
PROVIDER: S-EPMC4351439 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Worldwide monitoring programs of the invasive fruit pest Drosophila suzukii Matsumura (Diptera: Drosophilidae), using fermentation baits like apple cider vinegar (ACV), revealed a counterintuitive period of low trap catches during summer, followed by an autumn peak. In this study, we demonstrate that ACV baited traps indeed provide a distorted image of the D. suzukii population dynamics as it is possible to capture higher numbers during this "low capture period" with synthetic lures. It was hypothesised that the preference of D. suzukii populations for fermentation cues like ACV is most pronounced during autumn, winter and spring, while the flies prefer fresh fruit cues during summer and that this seasonal preference is related to the changing physiology of the flies over the season. To test this hypothesis, the preference between fermentation cues (ACV) and host fruits (strawberries) and the effect of physiology (sex, seasonal morphology and feeding, mating and reproductive status) was investigated both in olfactometer laboratory experiments and a year-round field preference experiment. In olfactometer experiments we demonstrated that protein deprived females, virgin females with a full complement of unfertilised eggs and males show a strong preference for fermentation cues while fully fed reproductive summer morph females generally prefer fruit cues. These findings indicate that D. suzukii is attracted to fermentation volatiles in search of (protein-rich) food and to fruit volatiles in search of oviposition substrates. Winter morph and starved females displayed indiscriminating olfactory behaviour. In the field preference experiment, the hypothesised seasonal shift between fermentation and fruit cues was confirmed. This shift appeared to be highly temperature-related and was similarly observed for summer and winter morphs.
| S-EPMC6681279 | biostudies-literature
Project description:The agricultural pest Drosophila suzukii differs from most other Drosophila species in that it lays eggs in ripe, rather than overripe, fruit. Previously, we showed that changes in bitter taste sensation accompanied this adaptation (Dweck et al., 2021). Here, we show that D. suzukii has also undergone a variety of changes in sweet taste sensation. D. suzukii has a weaker preference than Drosophila melanogaster for laying eggs on substrates containing all three primary fruit sugars: sucrose, fructose, and glucose. Major subsets of D. suzukii taste sensilla have lost electrophysiological responses to sugars. Expression of several key sugar receptor genes is reduced in the taste organs of D. suzukii. By contrast, certain mechanosensory channel genes, including no mechanoreceptor potential C, are expressed at higher levels in the taste organs of D. suzukii, which has a higher preference for stiff substrates. Finally, we find that D. suzukii responds differently from D. melanogaster to combinations of sweet and mechanosensory cues. Thus, the two species differ in sweet sensation, mechanosensation, and their integration, which are all likely to contribute to the differences in their egg-laying preferences in nature.
| S-EPMC9674340 | biostudies-literature
Project description:The survey data presented in this article provides information on risk management strategies in response to the invasive pest Drosophila suzukii (spotted wing drosophila) collected among Swiss fruit and wine growers. The survey covered grape, plum, berry and cherry growers and the years 2016, 2017 and 2018. Strategies to prevent or control Drosophila suzukii were collected at the variety level and information on perceived infestation levels as well as harvest losses was collected. In total, nine surveys were conducted, creating a unique panel dataset. Additionally, data was collected with regard to fruit growers' characteristics (e.g. age, gender) and farm characteristics (e.g. farm size, farm-level workforce, succession, insurance use). Risk preferences were elicited via a self-assessment of risk preferences and (for selected surveys) using a multiple price list. Additionally, (for selected surveys) locus of control and self-efficacy were evaluated via self-assessment questions.
| S-EPMC6487358 | biostudies-literature
Project description:How the evolution of olfactory genes correlates with adaption to new ecological niches is still a debated topic. We explored this issue in Drosophila suzukii, an emerging model that reproduces on fresh fruit rather than in fermenting substrates like most other Drosophila We first annotated the repertoire of odorant receptors (ORs), odorant binding proteins (OBPs), and antennal ionotropic receptors (aIRs) in the genomes of two strains of D. suzukii and of its close relative Drosophila biarmipes We then analyzed these genes on the phylogeny of 14 Drosophila species: whereas ORs and OBPs are characterized by higher turnover rates in some lineages including D. suzukii, aIRs are conserved throughout the genus. Drosophila suzukii is further characterized by a non-random distribution of OR turnover on the gene phylogeny, consistent with a change in selective pressures. In D. suzukii, we found duplications and signs of positive selection in ORs with affinity for short-chain esters, and loss of function of ORs with affinity for volatiles produced during fermentation. These receptors-Or85a and Or22a-are characterized by divergent alleles in the European and American genomes, and we hypothesize that they may have been replaced by some of the duplicated ORs in corresponding neurons, a hypothesis reciprocally confirmed by electrophysiological recordings. Our study quantifies the evolution of olfactory genes in Drosophila and reveals an array of genomic events that can be associated with the ecological adaptations of D. suzukii.
| S-EPMC5010897 | biostudies-literature
Project description:Specialization onto different host plants has been hypothesized to be a major driver of diversification in insects, and traits controlling olfaction have been shown to play a fundamental role in host preferences. A diverse set of olfactory genes control olfactory traits in insects, and it remains unclear whether specialization onto different hosts is likely to involve a nonrandom subset of these genes. Here, we test the role of olfactory genes in a novel case of specialization in Drosophila orena. We report the first population-level sample of D. orena on the West African island of Bioko, since its initial collection in Cameroon in 1975, and use field experiments and behavioral assays to show that D. orena has evolved a strong preference for waterberry (Syzygium staudtii). We then show that a nonrandom subset of genes controlling olfaction--those controlling odorant-binding and chemosensory proteins--have an enriched signature of positive selection relative to the rest of the D. orena genome. By comparing signatures of positive selection on olfactory genes between D. orena and its sister species, D. erecta we show that odorant-binding and chemosensory have evidence of positive selection in both species; however, overlap in the specific genes with evidence of selection in these two classes is not greater than expected by chance. Finally, we use quantitative complementation tests to confirm a role for seven olfactory loci in D. orena's preference for waterberry fruit. Together, our results suggest that D. orena and D. erecta have specialized onto different host plants through convergent evolution at the level of olfactory gene family, but not at specific olfactory genes.
| S-EPMC6121841 | biostudies-other
Project description:Yeasts play an important role in nutrition physiology and host attraction of many Drosophila species, and associations with various yeast species are documented for several drosophilid flies. The pest Drosophila suzukii (Matsumura) has a predominant association with the yeast Hanseniaspora uvarum. However, research has not been conducted on the nutritional physiology of the yeasts associated with D. suzukii (spotted wing drosophila). Therefore, in this study, we determined whether dietary yeast was nutritionally relevant and whether yeast species closely associated with D. suzukii positively affected life-history traits. Our results confirm a crucial role of dietary yeast in the larval development and survival of D. suzukii. Furthermore, we found specific effects of the closely associated yeast species H. uvarum and Candida sp. on larval survival. Observations of the egg-laying behaviour of D. suzukii on cherry fruits artificially colonised with different yeast species revealed that the number of eggs laid increased on fruits colonised with Candida sp. and Saccharomyces cerevisiae.
| S-EPMC5847167 | biostudies-literature
Project description:Drosophila suzukii Matsumura (Diptera: Drosophilidae) is a significant invasive pest in soft-skin fruits and berries in Asia, Europe, and North and South America. Many herbivorous insects use multiple cues for host selection, particularly olfactory and visual stimuli. The visual system of closely-related Drosophila melanogaster is well-documented, expressing strong sensitivity to short-wavelength colors (ultraviolet to green) and only limited sensitivity to long-wavelength colors (red to infrared). Our results suggest that D. suzukii have limited ability to distinguish red consistent with visual sensitivity range within the melanogaster subgroup. We propose that color contrast rather than color appearance may be of greater importance in orientation and attraction. We propose that differences in reflectance between light wavelengths important for color opponency are key to color discrimination to provide color contrast between foreground and background, as occurs between fruit and foliage, during host-finding.
| S-EPMC6831584 | biostudies-literature
Project description:BackgroundThe bushbuck, Tragelaphus scriptus, is a widespread and ecologically diverse ungulate species complex within the spiral-horned antelopes. This species was recently found to consist of two genetically divergent but monophyletic lineages, which are paraphyletic at mitochondrial (mt)DNA owing to an ancient interspecific hybridization event. The Scriptus lineage (T. s. scriptus) inhabits the north-western half of the African continent while Sylvaticus (T. s. sylvaticus) is found in the south-eastern half. Here we test hypotheses of historical demography and adaptation in bushbuck using a higher-resolution framework, with four nuclear (MGF, PRKCI, SPTBN, and THY) and three new mitochondrial markers (cytochrome b, 12S rRNA, and 16S rRNA).MethodsGenealogies were reconstructed for the mitochondrial and nuclear data sets, with the latter dated using fossil calibration points. We also inferred the demographic history of Scriptus and Sylvaticus using coalescent-based methods. To obtain an overview of the origins and ancestral colonisation routes of ancestral bushbuck sequences across geographic space, we conducted discrete Bayesian phylogeographic and statistical dispersal-vicariance analyses on our nuclear DNA data set.ResultsBoth nuclear DNA and mtDNA support previous findings of two genetically divergent Sylvaticus and Scriptus lineages. The three mtDNA loci confirmed 15 of the previously defined haplogroups, including those with convergent phenotypes. However, the nuclear tree showed less phylogenetic resolution at the more derived parts of the genealogy, possibly due to incomplete lineage sorting of the slower evolving nuclear genome. The only exception to this was the montane Menelik's bushbuck (Sylvaticus) of the Ethiopian highlands, which formed a monophyletic group at three of four nuclear DNA loci. We dated the coalescence of the two lineages to a common ancestor ∼2.54 million years ago. Both marker sets revealed similar demographic histories of constant population size over time. We show that the bushbuck likely originated in East Africa, with Scriptus dispersing to colonise suitable habitats west of the African Rift and Sylvaticus radiating from east of the Rift into southern Africa via a series of mainly vicariance events.DiscussionDespite lower levels of genetic structure at nuclear loci, we confirmed the independent evolution of the Menelik's bushbuck relative to the phenotypically similar montane bushbuck in East Africa, adding further weight to previous suggestions of convergent evolution within the bushbuck complex. Perhaps the most surprising result of our analysis was that both Scriptus and Sylvaticus populations remained relatively constant throughout the Pleistocene, which is remarkable given that this was a period of major climatic and tectonic change in Africa, and responsible for driving the evolution of much of the continent's extant large mammalian diversity.
| S-EPMC6476403 | biostudies-literature
Project description:The evolution of animal behaviour is poorly understood1,2. Despite numerous correlations between interspecific divergence in behaviour and nervous system structure and function, demonstrations of the genetic basis of these behavioural differences remain rare3-5. Here we develop a neurogenetic model, Drosophila sechellia, a species that displays marked differences in behaviour compared to its close cousin Drosophila melanogaster6,7, which are linked to its extreme specialization on noni fruit (Morinda citrifolia)8-16. Using calcium imaging, we identify olfactory pathways in D. sechellia that detect volatiles emitted by the noni host. Our mutational analysis indicates roles for different olfactory receptors in long- and short-range attraction to noni, and our cross-species allele-transfer experiments demonstrate that the tuning of one of these receptors is important for species-specific host-seeking. We identify the molecular determinants of this functional change, and characterize their evolutionary origin and behavioural importance. We perform circuit tracing in the D. sechellia brain, and find that receptor adaptations are accompanied by increased sensory pooling onto interneurons as well as species-specific central projection patterns. This work reveals an accumulation of molecular, physiological and anatomical traits that are linked to behavioural divergence between species, and defines a model for investigating speciation and the evolution of the nervous system.
| S-EPMC7100913 | biostudies-literature
Project description:Novel methodology is presented for indexing the relative potential of hosts to function as resources. A Host Potential Index (HPI) was developed as a practical framework to express relative host potential based on combining results from one or more independent studies, such as those examining host selection, utilization, and physiological development of the organism resourcing the host. Several aspects of the HPI are addressed including: 1) model derivation; 2) influence of experimental design on establishing host rankings for a study type (no choice, two-choice, and multiple-choice); and, 3) variable selection and weighting associated with combining multiple studies. To demonstrate application of the HPI, results from the interactions of spotted wing drosophila (SWD), Drosophila suzukii Matsumura (Diptera: Drosophilidae), with seven "reported" hosts (blackberries, blueberries, sweet cherries, table grapes, peaches, raspberries, and strawberries) in a postharvest scenario were analyzed. Four aspects of SWD-host interaction were examined: attraction to host volatiles; population-level oviposition performance; individual-level oviposition performance; and key developmental factors. Application of HPI methodology indicated that raspberries ( (mean)HPIvaried ?=?301.9±8.39; rank 1 of 7) have the greatest potential to serve as a postharvest host for SWD relative to the other fruit hosts, with grapes ( (mean)HPIvaried ?=?232.4±3.21; rank 7 of 7) having the least potential.
| S-EPMC3625224 | biostudies-literature