Evolution of Insect Olfaction

Neuroethology utilizes a wide range of multidisciplinary approaches to decipher neural correlates of natural behaviors associated with an animal's ecological niche. By placing emphasis on comparative analyses of adaptive and evolutionary trends across species, a neuroethological perspective is uniquely suited to uncovering general organizational and biological principles that shape the function and anatomy of the nervous system. In this review, we focus on the application of neuroethological principles in the study of insect olfaction and discuss how ecological environment and other selective pressures influence the development of insect olfactory neurobiology, not only informing our understanding of olfactory evolution but also providing broader insights into sensory processing

Olfactory Proxy Detection of Dietary Antioxidants in Drosophila

SummaryBackgroundDietary antioxidants play an important role in preventing oxidative stress. Whether animals in search of food or brood sites are able to judge the antioxidant content, and if so actively seek out resources with enriched antioxidant content, remains unclear.ResultsWe show here that the vinegar fly Drosophila melanogaster detects the presence of hydroxycinnamic acids (HCAs)—potent dietary antioxidants abundant in fruit—via olfactory cues. Flies are unable to smell HCAs directly but are equipped with dedicated olfactory sensory neurons detecting yeast-produced ethylphenols that are exclusively derived from HCAs. These neurons are housed on the maxillary palps, express the odorant receptor Or71a, and are necessary and sufficient for proxy detection of HCAs. Activation of these neurons in adult flies induces positive chemotaxis, oviposition, and increased feeding. We further demonstrate that fly larvae also seek out yeast enriched with HCAs and that larvae use the same ethylphenol cues as the adults but rely for detection upon a larval unique odorant receptor (Or94b), which is co-expressed with a receptor (Or94a) detecting a general yeast volatile. We also show that the ethylphenols act as reliable cues for the presence of dietary antioxidants, as these volatiles are produced—upon supplementation of HCAs—by a wide range of yeasts known to be consumed by flies.ConclusionsFor flies, dietary antioxidants are presumably important to counteract acute oxidative stress induced by consumption or by infection by entomopathogenic microorganisms. The ethylphenol pathway described here adds another layer to the fly’s defensive arsenal against toxic microbes

Dopamine drives Drosophila sechellia adaptation to its toxic host

Many insect species are host-obligate specialists. The evolutionary mechanism driving the adaptation of a species to a toxic host is, however, intriguing. We analyzed the tight association of Drosophila sechellia to its sole host, the fruit of Morinda citrifolia, which is toxic to other members of the melanogaster species group. Molecular polymorphisms in the dopamine regulatory protein Catsup cause infertility in D. sechellia due to maternal arrest of oogenesis. In its natural host, the fruit compensates for the impaired maternal dopamine metabolism with the precursor l-DOPA, resuming oogenesis and stimulating egg production. l-DOPA present in morinda additionally increases the size of D. sechellia eggs, what in turn enhances early fitness. We argue that the need of l-DOPA for successful reproduction has driven D. sechellia to become an M. citrifolia obligate specialist. This study illustrates how an insect's dopaminergic system can sustain ecological adaptations by modulating ontogenesis and development. DOI: http://dx.doi.org/10.7554/eLife.03785.00

Wild African Drosophila melanogaster are seasonal specialists on marula fruits

Although the vinegar fly Drosophila melanogaster isarguably the most studied organism on the planet,fundamental aspects of this species’ natural ecologyhave remained enigmatic [1]. We have here investigateda wild population of D. melanogaster from amopane forest in Zimbabwe. We find that these fliesare closely associated with marula fruit (Sclerocaryabirrea) and propose that this seasonally abundantand predominantly Southern African fruit is a keyancestral host of D. melanogaster. Moreover, whenfruiting, marula is nearly exclusively used byD. melanogaster, suggesting that these forest-dwellingD. melanogaster are seasonal specialists, in asimilar manner to, e.g., Drosophila erecta on screwpine cones [2]. We further demonstrate that themain chemicals released by marula activate odorantreceptors that mediate species-specific host choice(Or22a) [3, 4] and oviposition site selection (Or19a)[5]. The Or22a-expressing neurons—ab3A—respondstrongly to the marula ester ethyl isovalerate, a volatilerarely encountered in high amounts in other fruit.We also show that Or22a differs among African populationssampled from a wide range of habitats, inline with a function associated with host fruit usage.Flies from Southern Africa, most of which carry adistinct allele at the Or22a/Or22b locus, have ab3Aneurons that are more sensitive to ethyl isovaleratethan, e.g., European flies. Finally, we discuss thepossibility that marula, which is also a culturallyand nutritionally important resource to humans,may have helped the transition to commensalism inD. melanogaster

Influence of olfaction in host-selection behavior of the cassava whitefly Bemisia tabaci

Open Access Journal; Published online: 18 Nov 2021Cassava is a vital food-security crop in Sub-Saharan Africa. Cassava crops are, however, severely affected by viral diseases transmitted by members of the whitefly species complex Bemisia tabaci. We have here investigated the role of olfaction in host selection behavior of the cassava whitefly B. tabaci SSA-ESA biotype. Surprisingly, we find that the whiteflies appear to make little use of olfaction to find their favored host. The cassava whitely shows a highly reduced olfactory system, both at the morphological and molecular level. Whitefly antennae possess only 15 sensilla with possible olfactory function, and from the genome we identified just a handful of candidate chemoreceptors, including nine tuning odorant receptors, which would afford the whitefly with one of the smallest olfactomes identified from any insect to date. Behavioral experiments with host and non-host plants, as well as with identified specific volatiles from these sources, suggest that the few input channels present are primarily tuned toward the identification of unwanted features, rather than favored ones, a strategy quite unlike most other insects. The demonstrated repellence effect of specific volatile chemicals produced by certain plants unflavored by whiteflies suggests that intercropping with these plants could be a viable strategy to reduce whitefly infestations in cassava fields

Decoding odor quality and intensity in the Drosophila brain

To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information

The Cayman Crab Fly Revisited — Phylogeny and Biology of Drosophila endobranchia

BACKGROUND: The majority of all known drosophilid flies feed on microbes. The wide spread of microorganisms consequently mean that drosophilids also can be found on a broad range of substrates. One of the more peculiar types of habitat is shown by three species of flies that have colonized land crabs. In spite of their intriguing lifestyle, the crab flies have remained poorly studied. Perhaps the least investigated of the three crab flies is the Cayman Island endemic Drosophila endobranchia. Apart from its life cycle very little is known about this species, including its phylogenetic position, which has remained unresolved due to a cryptic set of characteristics. PRINCIPAL FINDINGS: Based on molecular data, corroborated by a re-analysis of the morphological make up, we have resolved the phylogenetic position of D. endobranchia and show that it somewhat surprisingly belongs to the large Neotropical repleta radiation, and should be considered as an aberrant member of the canalinea species group. Furthermore we also provide additional data on the behavior of these remarkable flies. CONCLUSION: Our findings reveal that the two Caribbean crab flies are not as distantly related as first thought, as both species are members of the derived repleta radiation. That this lineage has given rise to two species with the same odd type of breeding substrate is curious and prompts the question of what aspects of their shared ancestry has made these flies suitable for a life on (and inside) land crabs. Knowledge of the phylogenetic position of D. endobranchia will allow for comparative explorations and will aid in efforts aimed at understanding processes involved in drastic host shifts and extreme specialization

Towards plant-odor-related olfactory neuroethology in Drosophila

Drosophila melanogaster is today one of the three foremost models in olfactory research, paralleled only by the mouse and the nematode. In the last years, immense progress has been achieved by combining neurogenetic tools with neurophysiology, anatomy, chemistry, and behavioral assays. One of the most important tasks for a fruit fly is to find a substrate for eating and laying eggs. To perform this task the fly is dependent on olfactory cues emitted by suitable substrates as e.g. decaying fruit. In addition, in this area, considerable progress has been made during the last years, and more and more natural and behaviorally active ligands have been identified. The future challenge is to tie the progress in different fields together to give us a better understanding of how a fly really behaves. Not in a test tube, but in nature. Here, we review our present state of knowledge regarding Drosophila plant-odor-related olfactory neuroethology to provide a basis for new progress