Peláez Julianne N, Bernstein Susan, Okoro Judith, Rodas Esteban, Liang Irene, Leipertz Anna, Marion-Poll Frédéric, Whiteman Noah K
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
Evolution, Genomes, Behaviour and Ecology, IDEEV, CNRS, Université Paris-Saclay, IRD, Gif-sur-Yvette, France.
bioRxiv. 2024 Feb 29:2024.02.27.582299. doi: 10.1101/2024.02.27.582299.
Plant secondary metabolites pose a challenge for generalist herbivorous insects because they are not only potentially toxic, they also may trigger aversion. On the contrary, some highly specialized herbivorous insects evolved to use these same compounds as 'token stimui' for unambiguous determination of their host pants. Two questions that emerge from these observations are how recently derived herbivores evolve to overcome this aversion to plant secondary metabolites and the extent to which they evolve increased attraction to these same compounds. In this study, we addressed these questions by focusing on the evolution of bitter taste preferences in the herbivorous drosophilid , which is phylogenetically nested deep in the paraphyletic . We measured behavioral and neural responses of and a set of non-herbivorous species representing a phylogenetic gradient (, , and ) towards host- and non-host derived bitter plant compounds. We observed that evolved a shift in bitter detection, rather than a narrow shift towards glucosinolates, the precursors of mustard-specific defense compounds. In a dye-based consumption assay, exhibited shifts in aversion toward the non-mustard bitter, plant-produced alkaloids caffeine and lobeline, and reduced aversion towards glucosinolates, whereas the non-herbivorous species each showed strong aversion to all bitter compounds tested. We then examined whether these changes in bitter preferences of could be explained by changes in sensitivity in the peripheral nervous system and compared electrophysiological responses from the labellar sensilla of , , and . Using scanning electron microscopy, we also created a map of labellar sensilla in and We assigned each sensillum to a functional sensilla class based on their morphology and initial response profiles to bitter and sweet compounds. Despite a high degree of conservation in the morphology and spatial placement of sensilla between , electrophysiological studies revealed that had reduced sensitivity to glucosinolates to varying degrees. We found this reduction only in I type sensilla. Finally, we speculate on the potential role that evolutionary genetic changes in gustatory receptors between and may play in driving these patterns. Specifically, we hypothesize that the evolution of bitter receptors expressed in I type sensilla may have driven the reduced sensitivity observed in , and ultimately, its reduced bitter aversion. The system showcases the importance of reduced aversion to bitter defense compounds in relatively young herbivorous lineages, and how this may be achieved at the molecular and physiological level.
植物次生代谢产物对多食性食草昆虫构成了挑战，因为它们不仅可能有毒，还可能引发厌恶反应。相反，一些高度特化的食草昆虫进化出利用这些相同的化合物作为“信号刺激物”，以明确识别它们的寄主植物。从这些观察中产生的两个问题是，新近分化出的食草动物如何进化以克服对植物次生代谢产物的这种厌恶，以及它们在多大程度上进化出对这些相同化合物增强的吸引力。在这项研究中，我们通过关注食草性果蝇苦味偏好的进化来解决这些问题，果蝇在系统发育上嵌套于并系群的深处。我们测量了果蝇以及一组代表系统发育梯度的非食草性物种（黑腹果蝇、拟暗果蝇和海德氏果蝇）对寄主和非寄主来源的苦味植物化合物的行为和神经反应。我们观察到果蝇进化出了苦味检测的转变，而不是向芥子特异性防御化合物的前体硫代葡萄糖苷的狭窄转变。在基于染料的摄食试验中，果蝇对非芥子苦味、植物产生的生物碱咖啡因和洛贝林的厌恶发生了转变，对硫代葡萄糖苷的厌恶降低，而每个非食草性物种对所有测试的苦味化合物都表现出强烈的厌恶。然后，我们研究了果蝇苦味偏好的这些变化是否可以通过外周神经系统敏感性的变化来解释，并比较了果蝇、黑腹果蝇和拟暗果蝇唇叶感器的电生理反应。使用扫描电子显微镜，我们还绘制了果蝇和黑腹果蝇唇叶感器的图谱。我们根据它们的形态以及对苦味和甜味化合物的初始反应谱将每个感器归类到一个功能感器类别。尽管果蝇和黑腹果蝇之间感器的形态和空间位置高度保守，但电生理研究表明果蝇对硫代葡萄糖苷的敏感性有不同程度的降低。我们只在I型感器中发现了这种降低。最后，我们推测果蝇和黑腹果蝇之间味觉受体的进化遗传变化在驱动这些模式中可能发挥的潜在作用。具体来说，我们假设在I型感器中表达的苦味受体的进化可能导致了果蝇中观察到的敏感性降低，最终导致其苦味厌恶降低。果蝇系统展示了在相对年轻的食草谱系中降低对苦味防御化合物厌恶的重要性，以及这在分子和生理水平上是如何实现的。
