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Wertheim, B.

Publications and source records attributed to Wertheim, B..

10 recordsLinked to original sources

Sociability is a multidimensional trait in Drosophila melanogaster

Sociability--the propensity of an individual to engage in group activities--is a trait present in all social species. In humans and many animals, sociability varies between individuals yet remains consistent across contexts, qualifying it as a personality trait. Sociability influences health and physiology, but the mechanisms underlying sociability and its inter-individual variation remain poorly understood. The genetically tractable fruit fly, Drosophila melanogaster, is increasingly used to study social behavior and exhibits a wide range of sociability phenotypes. However, previous studies have relied on distinct behavioral paradigms, limiting cross-context comparisons and motivating a more extensive characterization of sociability in this species. Here, we quantified sociability in D. melanogaster using a multidimensional approach encompassing three paradigms that capture engagement in group activities across contexts: (1) preference for communal versus solitary egg-laying, (2) egg-laying latency in a group, and (3) frequency and duration of spontaneous social interactions and interindividual distance. We assessed these behaviors in 105 lines of the Drosophila Genetic Reference Panel and observed substantial variation in responses to conspecific presence across paradigms. Sociability-related behaviors differed between genetically distinct lines, indicating a genetic component. However, the three sociability traits were uncorrelated, demonstrating that sociability in D. melanogaster is multidimensional. These findings suggest that sociability is not governed by a single central mechanism, but instead arises from multiple context-dependent pathways.

animal behavior and cognition↗

Migration patterns and hybridization within the Asian stonechat complex in response to a major geographical barrier

Long-distance avian migration is thought to be under strong natural selection. Facing geographical barriers, migrants display various patterns considered to be adaptive. For example, they may detour along either side around the barrier or cross it, requiring specialized behavioral adaptations. Variations within closely related taxa are excellent sources for understanding the evolutionary background of migration and how barriers are shaping migration routes. In Asia, some species are assumed to have a migratory divide in response to the major geographical barrier, the Qinghai-Tibet Plateau (QTP), including the stonechat taxa (Siberian Stonechat Saxicola maurus maurus and Amur Stonechat S. stejnegeri). As they detour along either side of the QTP, these taxa are believed to disfavor a crossing over the highland. However, the more southernly distributed Tibetan Stonechat (S. m. przewalskii) breeds on the QTP, suggesting adaptation to high elevation. To investigate migration patterns and the potentially associated genetic differences, we studied migration routes and population genetics of four populations around the assumed migratory divide in Russia and Mongolia, and of one from the QTP in China. Our results confirmed the existence of a migratory divide between maurus and stejnegeri, albeit with extensive hybridization. We observed both the hypothesized western and eastern routes, but also found individuals employing intermediate routes crossing the QTP, of which two-thirds were clear hybrids. Meanwhile, przewalskii followed a highland-crossing route and was genetically differentiated from maurus and stejnegeri. The diverse migration routes among Asian stonechats show differential responses towards the geographical barrier. The intermediate route may be associated with hybridization, and its conditional viability may facilitate gene flow between maurus and stejnegeri. The Asian stonechat complex thus offers great opportunities for novel research of the genetics and evolution of migration. The specific evolutionary background associated with inhabiting and crossing the QTP can offer new perspectives in this field. Teaser textMigratory divides can arise in birds because alternative routes around migratory barriers would select for behaviors to restrict hybridization. Hybrids of parental types that employ alternative routes are hypothesized to embark on intermediate routes that would expose them to suboptimal conditions, resulting in post-zygotic reproductive isolation. However, this hypothesis is challenged when a sister taxon actually breeds on the geographical barrier. This is the case in the Asian stonechat complex that breeds near or on the Qinghai-Tibet Plateau (QTP), the roof of the world. We demonstrated a migratory divide in central Siberia to Mongolia for race maurus and stejnegeri, yet showed also evidence for extensive hybridization. Hybrids migrated along a newly discovered intermediate route, seemingly viable and overlaps with the migration trajectory of race przewalskii over the eastern part of the QTP. The Asian migratory divide relative to the QTP thus provided new insights to the evolution of landbird migration.

evolutionary biology↗

Footprints of worldwide adaptation in structured populations of D. melanogaster through the expanded DEST 2.0 genomic resource

Large scale genomic resources can place genetic variation into an ecologically informed context. To advance our understanding of the population genetics of the fruit fly Drosophila melanogaster, we present an expanded release of the community-generated population genomics resource Drosophila Evolution over Space and Time (DEST 2.0; https://dest.bio/). This release includes 530 high-quality pooled libraries from flies collected across six continents over more than a decade (2009-2021), most at multiple time points per year; 211 of these libraries are sequenced and shared here for the first time. We used this enhanced resource to elucidate several aspects of the species demographic history and identify novel signs of adaptation across spatial and temporal dimensions. We showed that patterns of secondary contact, originally characterized in North America, are replicated in South America and Australia. We also found that the spatial genetic structure of populations is stable over time, but that drift due to seasonal contractions of population size causes populations to diverge over time. We identified signals of adaptation that vary between continents in genomic regions associated with xenobiotic resistance, consistent with independent adaptation to common pesticides. Moreover, by analyzing samples collected during spring and fall across Europe, we provide new evidence for seasonal adaptation related to loci associated with pathogen response. Furthermore, we have also released an updated version of the DEST genome browser. This is a useful tool for studying spatio-temporal patterns of genetic variation in this classic model system.

evolutionary biology↗

Mitochondrial variation in Anopheles gambiae and An. coluzzii: phylogeographic legacy of species isolation and mito-nuclear associations with metabolic resistance to pathogens and insecticides

Mitochondrial DNA (mtDNA) has been a popular marker in phylogeography, phylogeny, and molecular ecology, but its complex evolution is increasingly recognized. Here, we investigated mtDNA variation in An. gambiae and An. coluzzii, in perspective with other species in the Anopheles gambiae complex (AGC), by assembling the mitogenomes of 1219 mosquitoes across Africa. The mtDNA phylogeny of the AGC was consistent with a previously reported highly reticulated evolutionary history, revealing important discordances with the species tree. The three most widespread species (An. gambiae, An. coluzzii, An. arabiensis), known for extensive historical introgression, could not be discriminated based on mitogenomes. Furthermore, a monophyletic clustering of the three salt-water tolerant species (An. merus, An. melas, An. bwambae) in the AGC also suggested that introgression and possibly selection shaped mtDNA evolution. MtDNA variation in An. gambiae and An. coluzzii across Africa revealed significant partitioning among populations and species. A peculiar mtDNA lineage found predominantly in An. coluzzii and in the hybrid taxon of the African "far-west" exhibited divergence comparable to the inter-species divergence in the AGC, with a geographic distribution matching closely An. coluzziis geographic range. This phylogeographic relict of the An. coluzzii and An. gambiae split was associated with population and species structuration, but not with Wolbachia occurrence. The lineage was significantly associated with SNPs in the nuclear genome, particularly in genes associated with pathogen and insecticide resistance. These findings underline the mito-nuclear coevolution history and the role played by mitochondria in shaping metabolic responses to pathogens and insecticide in Anopheles.

evolutionary biology↗

Insights into the microbial strain mediated impact on pest insect development

Molecular analyses of host-associated microorganisms have demonstrated the essential role that the microbiome plays in host development. Approaches targeting the sequencing of ribosomal genes have successfully identified key species of the host-associated microbiome. However, it remains unclear to what extent the strain-specific characteristics influence the outcome of the host-microbiome interactions. This is particularly important for insect pests, where microbial species might be used as targets for biocontrol purposes. Understanding strain-level variation represents thus a crucial step in determining the microbial impact on hosts. To investigate the microbial strain-level effects on an invasive insect pest, Drosophila suzukii, we compared the impact of monocultures and cocultures of different bacterial and yeast strains. We investigated whether different strains of Gluconobacter and Pichia differentially influenced the larval development of the pest. Fly trait measurements demonstrated beneficial, although variable, impact of these microbial strains on the fitness of suzukii. Using cocultures of microbial strains, we found that in some combinations, the beneficial effects were intermediate between those of the respective monocultures. In contrast, in other cases, strong inhibitory effects were observed. Hence, our study reports that strain-level effects within species are present in D. suzukii, reinforcing the importance of assessing the impact of associated microbiota on pest insects at the strain level. HighlightsO_LIMicrobial strains make up an essential part of the diversity of an insect hosts C_LIO_LICharacterizing and accounting for strain-specific impact on a pests life-history traits and different combinations of strains constitute an important step in our understanding of the pest management strategies. C_LIO_LIWe investigated whether there was any strain-specific impact of bacteria and yeasts on the larval development of a frugivorous pest. C_LIO_LIWe observed that strains varied in their impact, both as monocultures and cocultures, indicating their importance in modifying the host ecology. C_LIO_LIOur study adds to the growing literature on the importance of strains in pest insects. C_LI

ecology↗

More persistent bacterial than fungal associations in the microbiota of a pest

The invasive fly Drosophila suzukii is a pest that can infest a diverse range of intact, ripening fruits, using its serrated ovipositor. This constitutes a different niche compared to the rotting fruits its ancestors use, especially because these intact fruits have limited quantities of microbes and soluble nutrients for the developing larvae. To investigate the potential role of microbial associations in the niche expansion of this invasive fly, we characterized the bacterial and fungal communities of D. suzukii and various wild fruits from which they developed. To assess cross-generational microbial associations, we also lab-reared fly populations and characterized their microbial communities. Diversity metrics of microbial communities differed significantly between flies and fruits. Different fruit types varied substantially in microbial composition, while flies showed relatively uniform bacterial communities, irrespective of the fruit source they developed on. After lab-rearing, bacterial communities still showed considerable overlap with those of wild flies. Fungal communities of flies and fruits showed larger resemblance, with a substantial overlap between wild flies and the corresponding fruits on which they had developed. Our study thus reports that the fungal community structure in these pests largely reflects those on the breeding substrates, while these flies might have formed more persistent associations with bacteria and transmit these across generations rather than obtaining them from their food source.

ecology↗

Social modulation of oogenesis and egg-laying in Drosophila melanogaster

Being part of a group facilitates cooperation between group members, but also creates competition for limited resources. This conundrum is problematic for gravid females who benefit from being in a group, but whose future offspring may struggle for access to nutrition in larger groups. Females should thus modulate their reproductive output depending on their social context. Although social-context dependent modulation of reproduction is documented in a broad range of species, its underlying mechanisms and functions are poorly understood. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The tractability of the genetics of this species allows dissecting the mechanisms underlying physiological adaptation to their social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster in group than alone, females appear to reduce competition between offspring and increase their likelihood of survival. In addition, females in a group lay their eggs during the light phase of the day, while isolated females lay them during the night. We show that responses to the presence of others are determined by vision through the motion detection pathway and that flies from any sex, mating status or species can trigger these responses. The mechanisms of this modulation of egg-laying by group is connected to a lifting of the inhibition of light on oogenesis and egg-laying by stimulating hormonal pathways involving juvenile hormone. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings represent a protosocial mechanism in a species considered solitary that may have been the target of selection for the evolution of more complex social systems.

animal behavior and cognition↗

Timing of increased temperature sensitivity coincides with nervous system development in winter moth embryos

Climate change is rapidly altering the environment and many species will need to genetically adapt their seasonal timing to keep up with these changes. Insect development rate is largely influenced by temperature, but we know little about the mechanisms underlying temperature sensitivity of development. Here we investigate seasonal timing of egg hatching in the winter moth, one of the few species which has been found to genetically adapt to climate change, likely through selection on temperature sensitivity of egg development rate. To study when during development winter moth embryos are most sensitive to changes in ambient temperature, we gave eggs an increase or decrease in temperature at different moments during their development. We measured their developmental progression and timing of egg hatching, and used fluorescence microscopy to construct a timeline of embryonic development for the winter moth. We found that egg development rate responded more strongly to temperature once embryos were in the fully extended germband stage. This is the phylotypic stage at which all insect embryos have developed a rudimentary nervous system. Furthermore, at this stage timing of ecdysone signaling determines developmental progression, which could act as an environment dependent gateway. Intriguingly, this may suggest that, from the phylotypic stage onward, insect embryos can start to integrate internal and environmental stimuli to actively regulate important developmental processes. As we found evidence that there is genetic variation for temperature sensitivity of egg development rate in our study population, such regulation could be a target of selection imposed by climate change.

evolutionary biology↗

DROP: Molecular voucher database for identification of Drosophila parasitoids

Molecular identification is increasingly used to speed up biodiversity surveys and laboratory experiments. However, many groups of organisms cannot be reliably identified using standard databases such as GenBank or BOLD due to lack of sequenced voucher specimens identified by experts. Sometimes a large number of sequences are available, but with too many errors to allow identification. Here we address this problem for parasitoids of Drosophila by introducing a curated open-access molecular reference database, DROP (Drosophila parasitoids). Identifying Drosophila parasitoids is challenging and poses a major impediment to realize the full potential of this model system in studies ranging from molecular mechanisms to food webs, and in biological control of Drosophila suzukii. In DROP (http://doi.org/10.5281/zenodo.4519656), genetic data are linked to voucher specimens and, where possible, the voucher specimens are identified by taxonomists and vetted through direct comparison with primary type material. To initiate DROP, we curated 154 laboratory strains, 856 vouchers, 554 DNA sequences, 16 genomes, 14 transcriptomes, and 6 proteomes drawn from a total of 183 operational taxonomic units (OTUs): 114 described Drosophila parasitoid species and 69 provisional species. We found species richness of Drosophila parasitoids to be heavily underestimated and provide an updated taxonomic catalogue for the community. DROP offers accurate molecular identification and improves cross-referencing between individual studies that we hope will catalyze research on this diverse and fascinating model system. Our effort should also serve as an example for researchers facing similar molecular identification problems in other groups of organisms.

genomics↗

Does Drosophila sechellia escape parasitoid attack by feeding on a toxic resource?

Host shifts can drastically change the selective pressures that animals experience from their environment. Drosophila sechellia is a species restricted to the Seychelles islands, where it specialized on the fruit Morinda citrifolia (noni). This fruit is known to be toxic to closely related Drosophila species, including D. melanogaster and D. simulans, releasing D. sechellia from interspecific competition when breeding on this substrate. Previously, we showed that D. sechellia is unable to mount an effective immunological response against wasp attack, while the closely-related species can defend themselves from parasitoid attack by melanotic encapsulation. We hypothesized that this inability constitutes a trait loss due to a reduced risk of parasitoid attack in noni. Here we present a field study aimed to test the hypothesis that specialization on noni has released D. sechellia from the antagonistic interaction with its larval parasitoids. Our results from the field survey indicate that D. sechellia was found in ripe noni, whereas another Drosophila species, D. malerkotliana, was present in unripe and rotting stages. Parasitic wasps of the species Leptopilina boulardi emerged from rotten noni, where D. malerkotliana was the most abundant host. These results indicate that the specialization of D. sechellia on noni has indeed drastically altered its ecological interactions, leading to a relaxation in the selection pressure to maintain parasitoid resistance.

evolutionary biology↗