Amir Yassin

Recurrent specialization on a toxic fruit in an island Drosophila population

Significance Host plant specialization is a major cause of diversification in insects. The specialization of the fly Drosophila sechellia on the toxic fruits of noni has been a source of great scientific value, but selection is old enough that genetic variation does not seem useful in mapping the causative genes. On the island of Mayotte, we discovered a population of the related species Drosophila yakuba that is strongly associated with noni compared with generalist mainland populations. We then leveraged genomic variation to reconstruct the recent divergence history of this population and identify the potential targets of selection. Our top candidates included genes that confer tolerance to nonis toxin in D. sechellia. These findings establish a new model for recurrent ecological specialization. Recurrent specialization on similar host plants offers a unique opportunity to unravel the evolutionary and genetic mechanisms underlying dietary shifts. Recent studies have focused on ecological races belonging to the same species, but it is hard in many cases to untangle the role of adaptive introgression versus distinct mutations in facilitating recurrent evolution. We discovered on the island of Mayotte a population of the generalist fly Drosophila yakuba that is strictly associated with noni (Morinda citrifolia). This case strongly resembles Drosophila sechellia, a genetically isolated insular relative of D. yakuba whose intensely studied specialization on toxic noni fruits has always been considered a unique event in insect evolution. Experiments revealed that unlike mainland D. yakuba strains, Mayotte flies showed strong olfactory attraction and significant toxin tolerance to noni. Island females strongly discriminated against mainland males, suggesting that dietary adaptation has been accompanied by partial reproductive isolation. Population genomic analysis indicated a recent colonization (∼29 kya), at a time when year-round noni fruits may have presented a predictable resource on the small island, with ongoing migration after colonization. This relatively recent time scale allowed us to search for putatively adaptive loci based on genetic variation. Strong signals of genetic differentiation were found for several detoxification genes, including a major toxin tolerance locus in D. sechellia. Our results suggest that recurrent evolution on a toxic resource can involve similar historical events and common genetic bases, and they establish an important genetic system for the study of early stages of ecological specialization and speciation.

Within-species reproductive costs affect the asymmetry of satyrization in Drosophila.

Understanding how species interactions influence their distribution and evolution is a fundamental question in evolutionary biology. Theory suggests that asymmetric reproductive interference, in which one species induces higher reproductive costs on another species, may be more important in delimiting species boundaries than interspecific competition over resources. However, the underlying mechanisms of such asymmetry remain unclear. Here, we test whether differences in within‐species reproductive costs determine the between‐species asymmetry of costs using three allopatric Drosophila species belonging to the melanogaster subgroup. Our results support this hypothesis, especially in a pair of insular species. Males of one species that induce costs to their conspecific females led to a 5‐fold increase of heterospecific females mortality with dead flies bearing spectacular large melanized wounds on their genitalia. Males of the other species were harmful neither to their conspecific nor heterospecific females. Comparative studies of within‐species reproductive costs may therefore be a valuable tool for predicting between‐species interactions and community structures.

Drosophila as models to understand the adaptive process during invasion

The last few decades have seen a growing number of species invasions globally, including many insect species. In drosophilids, there are several examples of successful invasions, i.e. Zaprionus indianus and Drosophila subobscura some decades ago, but the most recent and prominent example is the invasion of Europe and North America by the pest species, Drosophila suzukii. During the invasive process, species often encounter diverse environmental conditions that they must respond to, either through rapid genetic adaptive shifts or phenotypic plasticity, or by some combination of both. Consequently, invasive species constitute powerful models for investigating various questions related to the adaptive processes that underpin successful invasions. In this paper, we highlight how Drosophila have been and remain a valuable model group for understanding these underlying adaptive processes, and how they enable insight into key questions in invasion biology, including how quickly adaptive responses can occur when species are faced with new environmental conditions.

A Variable Genetic Architecture of Melanic Evolution in Drosophila melanogaster

Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. In Drosophila melanogaster, high-altitude melanism has evolved in separate mountain ranges in sub-Saharan Africa, potentially as an adaptation to UV intensity. We investigated the genetic basis of this melanism in three populations using a new bulk segregant analysis mapping method. We identified 19 distinct QTL regions from nine mapping crosses, with several QTL peaks overlapping between two or all populations, and yet different crosses involving the same melanic population commonly yielded distinct QTL. The strongest QTL often overlapped well-known pigmentation genes, but we typically did not find wide signals of genetic differentiation (FST) between lightly and darkly pigmented populations at these genes. Instead, we found small numbers of highly differentiated SNPs at the probable causative genes. A simulation analysis showed that these patterns of polymorphism were consistent with selection on standing genetic variation. Overall, our results suggest that, even for potentially simpler traits like pigmentation, the complexity of adaptive trait evolution poses important challenges for QTL mapping and population genetic analysis.

Life history evolution and cellular mechanisms associated with increased size in high-altitude Drosophila.

Abstract Understanding the physiological and genetic basis of growth and body size variation has wide‐ranging implications, from cancer and metabolic disease to the genetics of complex traits. We examined the evolution of body and wing size in high‐altitude Drosophila melanogaster from Ethiopia, flies with larger size than any previously known population. Specifically, we sought to identify life history characteristics and cellular mechanisms that may have facilitated size evolution. We found that the large‐bodied Ethiopian flies laid significantly fewer but larger eggs relative to lowland, smaller‐bodied Zambian flies. The highland flies were found to achieve larger size in a similar developmental period, potentially aided by a reproductive strategy favoring greater provisioning of fewer offspring. At the cellular level, cell proliferation was a strong contributor to wing size evolution, but both thorax and wing size increases involved important changes in cell size. Nuclear size measurements were consistent with elevated somatic ploidy as an important mechanism of body size evolution. We discuss the significance of these results for the genetic basis of evolutionary changes in body and wing size in Ethiopian D. melanogaster.

Drosophilids (Diptera) from Mayotte island: an annotated list of species collected in 2013 and comments on the colonisation of Indian Ocean Islands

Summary. The Indian Ocean Islands are a most interesting region for evolutionary studies of terrestrial organisms and, among insects, the Drosophilidae family occupies a privileged position. The Comoros archipelago was, up to now, the least explored place among all the islands. We present here the results of a collection on one of the four main islands, Mayotte. From 4500 collected flies, 25 species were distinguished. The biology, ecology and biogeography of each species are discussed. Considering the extant known species from all islands, five evolutionary scenarios are proposed, ranging from the invasive, cosmopolitan, man-transported species to endemic species restricted to a single island. Some species raise a puzzling problem: despite having a very narrow and specialised ecological niche, they are broadly distributed on most islands and also on the African mainland.

Unresolved questions in genitalia coevolution: bridging taxonomy, speciation, and developmental genetics

Systematists and geneticists study biological diversity, but they use different approaches that rarely intersect. A very common pattern that is of interest for both researchers is the rapid evolution of genitalia, a trait of significant taxonomic utility in several sexually reproducing animal clades. The idea that both male and female genitalia are species-specific and play a role in reproductive isolation has long been controversial but has recently gained a renewed interest by speciation and developmental geneticists. Here, I highlight six unresolved questions in genitalia coevolution and I argue that systematists, with their well training in comparative morphology, usage of large and geographically diverse collections, and ability to apply molecular genetics techniques, can make important contributions. Such an extension of systematics into the speciation and developmental genetics realms is a promising opportunity to expand “integrative taxonomy” comparisons between DNA and morphology into more explanatory relationships between the two sources of taxonomic data.

Drosophila yakuba mayottensis, a new model for the study of incipient ecological speciation

ABSTRACT A full understanding of how ecological factors drive the fixation of genetic changes during speciation is obscured by the lack of appropriate models with clear natural history and powerful genetic toolkits. In a recent study, we described an early stage of ecological speciation in a population of the generalist species Drosophila yakuba (melanogaster subgroup) on the island of Mayotte (Indian Ocean). On this island, flies are strongly associated with the toxic fruits of noni (Morinda citrifolia) and show a partial degree of pre-zygotic reproductive isolation. Here, I mine the nuclear and mitochondrial genomes and provide a full morphological description of this population. Only 29 nuclear sites (< 4 × 10−7 of the genome) are fixed in this population and absent from 3 mainland populations and the closest relative D. santomea, but no mitochondrial or morphological character distinguish Mayotte flies from the mainland. This result indicates that physiological and behavioral traits may evolve faster than morphology at the early stages of speciation. Based on these differences, the Mayotte population is designated as a new subspecies, Drosophila yakuba mayottensis subsp. nov., and its strong potential in understanding the genetics of speciation and plant-insect interactions is discussed.

Oligogenic Adaptation, Soft Sweeps, and Parallel Melanic Evolution in Drosophila melanogaster

Unraveling the genetic architecture of adaptive phenotypic divergence is a fundamental quest in evolutionary biology. In Drosophila melanogaster, high-altitude melanism has evolved in separate mountain ranges in sub-Saharan Africa, potentially as an adaptation to UV intensity. We investigated the genetic basis of this melanism in three populations using a new bulk segregant analysis mapping method. Although hundreds of genes are known to affect cuticular pigmentation in D. melanogaster, we identified only 19 distinct QTLs from 9 mapping crosses, with several QTL peaks being shared among two or all populations. Surprisingly, we did not find wide signals of genetic differentiation (Fst) between lightly and darkly pigmented populations at these QTLs, in spite of the pronounced phenotypic difference in pigmentation. Instead, we found small numbers of highly differentiated SNPs at the probable causative genes. A simulation analysis showed that these patterns of polymorphism are consistent with selection on standing genetic variation (leading to “soft sweeps“). Our results thus support a role for oligogenic selection on standing genetic variation in driving parallel ecological adaptation.