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Shahandeh, M. P.

Publications and source records attributed to Shahandeh, M. P..

4 recordsLinked to original sources

Laboratory and wild Drosophila sechellia have conserved niche specialization phenotypes

A major challenge to investigating the proximate causes of ecological adaptation is the difficulty of studying the phenotypes of organisms in their natural environments. By necessity, many studies seeking to determine the genetic and cellular basis of adaptation therefore investigate potentially adaptive phenotypes under laboratory conditions where organisms are more easily experimentally manipulated. For laboratory models, it remains unclear if organisms maintained long term under laboratory conditions are representative of relatives in their natural environment. In recent years, Drosophila sechellia, a specialist species endemic to the Seychelles, has emerged as a (neuro)genetic model for studying the molecular basis of ecological adaptation. A multitude of studies have investigated the genetic and cellular basis of various aspects of this species specialization in a laboratory setting. However, the vast majority of these studies use laboratory strains of D. sechellia that were collected many decades ago, and have been maintained under conditions very different from their natural niche. Thus, it remains unclear if and how these strains resemble their wild counterparts. Here, we compare the phenotypes of these laboratory strains with recently-collected wild D. sechellia to ask if laboratory strains display a loss or degradation of phenotypes potentially involved in their specialization resulting from their long-term laboratory maintenance. Across several behavioral and anatomical phenotypes, we find a high degree of similarity between wild-caught and laboratory-maintained strains. Our results suggest that studies of the molecular mechanisms underlying D. sechellias phenotypes associated with specialization are likely representative of the evolution of these flies in the wild.

evolutionary biology↗

Evolution of circadian behavioral plasticity through cis-regulatory divergence of a neuropeptide gene

Widely-distributed species experience substantial environmental variation, which they often accommodate through behavioral plasticity. Although this ability is integral to fitness, we have little understanding of the mechanistic basis by which plasticity evolves. One factor that varies seasonally and by latitude is photoperiod (day length). Many organisms, including the cosmopolitan Drosophila melanogaster display circadian plasticity, adjusting to fluctuating photoperiod by varying the timing of their activity to coincide with changing dawn/dusk intervals1. Here, we compare D. melanogaster with the closely-related ecological specialist Drosophila sechellia, an equatorial island endemic that experiences minimal photoperiod variation, to investigate the molecular-genetic basis of circadian plasticity evolution2,3. We discover that D. sechellia displays exceptionally little circadian plasticity compared to D. melanogaster and other non-equatorial drosophilids. Through a screen of circadian mutants in D. melanogaster/D. sechellia hybrids, we identify a role of the neuropeptide Pigment-dispersing factor (Pdf) in this loss. While the coding sequence of Pdf is conserved, we show that Pdf has undergone cis-regulatory divergence in these drosophilids. We document species-specific temporal dynamic properties of Pdf RNA and protein expression, as well as Pdf neuron morphological plasticity, and demonstrate that modulating Pdf expression in D. melanogaster can influence the degree of behavioral plasticity. Furthermore, we find that the Pdf regulatory region exhibits signals of selection across populations of D. melanogaster from different latitudes. Finally, we provide evidence that plasticity confers a selective advantage for D. melanogaster at higher latitudes, while D. sechellia likely suffers fitness costs through reduced copulation success outside its range. Our work defines Pdf as a locus of evolution for circadian plasticity, which might have contributed to both D. melanogasters global distribution and D. sechellias habitat specialization. Moreover, together with spatial changes in Pdf expression reported in high-latitude drosophilid species4,5, our findings highlight this neuropeptide gene as a hotspot for circadian plasticity evolution.

evolutionary biology↗

Odor-gated oviposition behavior in an ecological specialist

Colonization of a novel ecological niche can require, or be driven by, evolution of an animals 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 fruits 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. sechellias host specialization.

animal behavior and cognition↗

The loci of behavioral evolution: Fas2 and tilB underlie differences in pupation site choice behavior between Drosophila melanogaster and D. simulans

The recent boom in genotype-phenotype studies has led to a greater understanding of the genetic architecture of a variety of traits. Among these traits, however, behaviors are still lacking, perhaps because they are complex and environmentally sensitive phenotypes, making them difficult to measure reliably for association studies. Here, we aim to fill this gap in knowledge with the results of a genetic screen for a complex behavioral difference, pupation site choice, between Drosophila melanogaster and D. simulans. In this study, we demonstrate a significant contribution of the X chromosome to the difference in pupation site choice behavior between these species. Using a panel of X-chromosome deletions, we screened the majority of the X chromosome for causal loci, and identified two regions that explain a large proportion of the X-effect. We then used gene disruptions and RNAi to demonstrate the substantial effects of a single gene within each region: Fas2 and tilB. Finally, we show that differences in tilB expression underlie species differences in pupation site choice behavior, and that generally, pupation site choice behavior appears to be correlated with relative expression of this gene. Our results suggest that even complex, environmentally sensitive behaviors may evolve through changes to loci with large phenotypic effects.\n\nAuthor summaryBehaviors are complex traits that involve sensory detection, higher level processing, and a coordinated output by the nervous system. This level of processing is highly susceptible to environmentally induced variation. Because of their complexity and sensitivity, behaviors are difficult to study; as a result, we have very little understanding of the genes involved in behavioral variation. In this study, we use common laboratory fruit fly model, Drosophila, to address this gap and dissect the genetic underpinnings of an environmentally sensitive behavior that differs between species. We find that a significant amount of the phenotypic difference between species is explained by a single chromosome. We further show that just two genes on this chromosome account for a large majority of its effect, suggesting that the genetic basis of complex behavioral evolution may be simpler than anticipated. For one of these genes, we show that a species-level difference in gene expression is associated with the difference in behavior. Our results contribute to a growing number of studies identifying the genetic components of behavior. Ultimately, we hope to use these data to better predict the number, types, and effects of genetic mutations necessary for complex behaviors to evolve.

genetics↗