Evolution of Multiple Sensory Systems Drives Novel Egg-Laying Behavior in the Fruit Pest Drosophila suzukii.

The rise of a pest species represents a unique opportunity to address how species evolve new behaviors and adapt to novel ecological niches [1]. We address this question by studying the egg-laying behavior of Drosophila suzukii, an invasive agricultural pest species that has spread from Southeast Asia to Europe and North America in the last decade [2]. While most closely related Drosophila species lay their eggs on decaying plant substrates, D. suzukii oviposits on ripening fruit, thereby causing substantial economic losses to the fruit industry [3-8]. D. suzukii has evolved an enlarged, serrated ovipositor that presumably plays a key role by enabling females to pierce the skin of ripe fruit [9]. Here, we explore how D. suzukii selects oviposition sites, and how this behavior differs from that of closely related species. We have combined behavioral experiments in multiple species with neurogenetics and mutant analysis in D. suzukii to show that this species has evolved a specific preference for oviposition on ripe fruit. Our results also establish that changes in mechanosensation, olfaction, and presumably gustation have contributed to this ecological shift. Our observations support a model in which the emergence of D. suzukii as an agricultural pest is the consequence of the progressive modification of several sensory systems, which collectively underlie a radical change in oviposition behavior.

Karageorgi M ，Bräcker LB ，Lebreton S ，Minervino C ，Cavey M ，Siju KP ，Grunwald Kadow IC ，Gompel N ，Prud'homme B ... -  《-》

Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii.

Although most Drosophila species lay eggs in overripe fruit, the agricultural pest Drosophila suzukii lays eggs in ripe fruit. We found that changes in bitter taste perception have accompanied this adaptation. We show that bitter-sensing mutants of Drosophila melanogaster undergo a shift in egg laying preference toward ripe fruit. D. suzukii has lost 20% of the bitter-sensing sensilla from the labellum, the major taste organ of the head. Physiological responses to various bitter compounds are lost. Responses to strawberry purées are lost from two classes of taste sensilla. Egg laying is not deterred by bitter compounds that deter other species. Profiling of labellar transcriptomes reveals reduced expression of several bitter Gr genes (gustatory receptors). These findings support a model in which bitter compounds in early ripening stages deter egg laying in most Drosophila species, but a loss of bitter response contributes to the adaptation of D. suzukii to ripe fruit.

Dweck HK ，Talross GJ ，Wang W ，Carlson JR ... -  《eLife》

Behavioral and Genomic Sensory Adaptations Underlying the Pest Activity of Drosophila suzukii.

Studying how novel phenotypes originate and evolve is fundamental to the field of evolutionary biology as it allows us to understand how organismal diversity is generated and maintained. However, determining the basis of novel phenotypes is challenging as it involves orchestrated changes at multiple biological levels. Here, we aim to overcome this challenge by using a comparative species framework combining behavioral, gene expression, and genomic analyses to understand the evolutionary novel egg-laying substrate-choice behavior of the invasive pest species Drosophila suzukii. First, we used egg-laying behavioral assays to understand the evolution of ripe fruit oviposition preference in D. suzukii compared with closely related species D. subpulchrella and D. biarmipes as well as D. melanogaster. We show that D. subpulchrella and D. biarmipes lay eggs on both ripe and rotten fruits, suggesting that the transition to ripe fruit preference was gradual. Second, using two-choice oviposition assays, we studied how D. suzukii, D. subpulchrella, D. biarmipes, and D. melanogaster differentially process key sensory cues distinguishing ripe from rotten fruit during egg-laying. We found that D. suzukii's preference for ripe fruit is in part mediated through a species-specific preference for stiff substrates. Last, we sequenced and annotated a high-quality genome for D. subpulchrella. Using comparative genomic approaches, we identified candidate genes involved in D. suzukii's ability to seek out and target ripe fruits. Our results provide detail to the stepwise evolution of pest activity in D. suzukii, indicating important cues used by this species when finding a host, and the molecular mechanisms potentially underlying their adaptation to a new ecological niche.

Durkin SM ，Chakraborty M ，Abrieux A ，Lewald KM ，Gadau A ，Svetec N ，Peng J ，Kopyto M ，Langer CB ，Chiu JC ，Emerson JJ ，Zhao L ... -  《-》

Structural and transcriptional evidence of mechanotransduction in the Drosophila suzukii ovipositor.

Drosophila suzukii is an invasive pest that prefers to lay eggs in ripening fruits, whereas most closely related Drosophila species exclusively use rotten fruit as oviposition site. This behaviour is allowed by an enlarged and serrated ovipositor that can pierce intact fruit skin, and by multiple contact sensory systems (mechanosensation and taste) that detect the optimal egg-laying substrates. Here, we tested the hypothesis that bristles present in the D. suzukii ovipositor tip contribute to these sensory modalities. Analysis of the bristle ultrastructure revealed that four different types of cuticular elements (conical pegs type 1 and 2, chaetic and trichoid sensilla) are present on the tip of each ovipositor plate. All of them have a poreless shaft and are innervated at their base by a single neuron that ends in a distal tubular body, thus resembling mechanosensitive structures. Fluorescent labelling in D. suzukii and D. melanogaster revealed that pegs located on the ventral side of the ovipositor tip are innervated by a single neuron in both species. RNA-sequencing profiled gene expression, notably sensory receptor genes of the terminalia of D. suzukii and of three other Drosophila species with changes in their ovipositor structure (from serrated to blunt ovipositor: Drosophila subpulchrella, Drosophila biarmipes and D. melanogaster). Our results revealed few species-specific transcripts and an overlapping expression of candidate mechanosensitive genes as well as the presence of some chemoreceptor transcripts. These experimental evidences suggest a mechanosensitive function for the D. suzukii ovipositor, which might be crucial across Drosophila species independently from ovipositor shape.

Crava CM ，Zanini D ，Amati S ，Sollai G ，Crnjar R ，Paoli M ，Rossi-Stacconi MV ，Rota-Stabelli O ，Tait G ，Haase A ，Romani R ，Anfora G ... -  《-》

Identification of potential mechanosensitive ion channels involved in texture discrimination during Drosophila suzukii egg-laying behaviour.

Drosophila suzukii (spotted wing drosophila) has become a major invasive insect pest of soft fruits in the America and Europe, causing severe yield losses every year. The female D. suzukii shows the oviposition preference for ripening or ripe fruit by cutting the hard skin with its serrated ovipositor. A recent study reported that mechanosensation is involved in the texture discrimination during egg-laying behaviour in D. suzukii. However, the underlying mechanism and molecular entity that control this behaviour are not known. The transient receptor potential (TRP) channels and degenerin/epithelial sodium channels (DEG/ENaC) are two candidate gene families of mechanically activated ion channels. Thus, we first identified TRP and DEG/ENaC genes in D. suzukii by bioinformatic analysis. Using transcriptome sequencing, we found that many TRP genes were expressed in the ovipositor in both D. suzukii and D. melanogaster, while some DEG/ENaCs showed species-specific expression patterns. Exposure to drugs targeting TRP and DEG/ENaC channels abolished the oviposition preference for harder texture in female D. suzukii. Therefore, mechanosensitive ion channels may play significant roles in the texture assessment of egg-laying behaviour in D. suzukii, which has promising implications to further research on the development of novel control measures.

Guo L ，Zhou ZD ，Mao F ，Fan XY ，Liu GY ，Huang J ，Qiao XM ... -  《-》