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 as compared to 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. Secondly, 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. Lastly, 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.

中文翻译：

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铃木果蝇有害生物活动的行为和基因组感觉适应

研究新型表型如何起源和进化是进化生物学领域的基础，因为它使我们能够理解生物多样性是如何产生和维持的。然而，确定新表型的基础是具有挑战性的，因为它涉及在多个生物学水平上精心策划的变化。在这里，我们旨在通过使用行为，基因表达和基因组分析相结合的比较物种框架来克服这一挑战，以了解入侵害虫物种果蝇果蝇的进化新型产卵底物-选择行为。首先，我们使用产卵行为试验来了解与密切相关的物种D. subpulchrella和D. biarmipes以及D. melanogaster相比，铃木D.中成熟果实产卵偏好的演变。我们显示D. subpulchrella和D. 双臂猿在成熟和腐烂的水果上都产卵，这表明向成熟水果偏爱的过渡是渐进的。其次，我们使用二选产卵子试验，研究了铃木D.subpulchrella，D。biarmipes和D. melanogaster如何在产卵过程中差异处理关键的感官线索，以区分腐烂果实和成熟果实。我们发现铃木D.对成熟果实的偏爱部分是通过特定物种对硬质基质的偏爱来介导的。最后，我们对D.subpulchrella的高质量基因组进行了测序和注释。使用比较基因组学方法，我们确定了与铃木毛虫寻找并靶向成熟果实的能力有关的候选基因。我们的结果提供了有关铃木D.有害生物活动逐步演变的详细信息，表明该物种在寻找寄主时会使用的重要线索，