Persyn Emma, Duyck Pierre-François, François Marie-Christine, Mille Christian, Jacob Vincent, Jacquin-Joly Emmanuelle
CIRAD, Université de la Réunion, UMR PVBMT, 7, ch. de l'IRAT, F-97410 Saint-Pierre, La Réunion, France; INRAE, Sorbonne Université, CNRS, IRD, UPEC, Université Paris Cité, Institute of Ecology & Environmental Sciences of Paris, Route de Saint-Cyr, F-78026 Versailles Cedex, France.
IAC, Institut Agronomique néo-Calédonien, Équipe ARBOREAL, Laboratoire d'Entomologie Appliquée, Station de Recherches Fruitières de Pocquereux, F-98880, La Foa, New Caledonia; CIRAD, UMR PVBMT, F-98488 Nouméa, New Caledonia.
Mol Phylogenet Evol. 2025 May;206:108322. doi: 10.1016/j.ympev.2025.108322. Epub 2025 Mar 4.
The insect olfactory system has evolved while guiding species to specific mating partners, different food sources, and oviposition sites. How species repertoires of odorant receptors (ORs), responsible for the detection of volatile cues, have been shaped by ecologically driven forces remains poorly understood. Due to several host switches back and forth throughout their evolutionary history, fruit flies of the Tephritidae family (Diptera) show highly diverse host preferences, making them good models to address this question. For instance, a comparative analysis of genomic and transcriptomic resources on a large variety of fruit fly species could provide statistical conclusions. Here, we used a RNAseq approach to identify the OR repertoires of thirteen Tephritidae species with different host ranges, namely Bactrocera curvipennis, Bactrocera dorsalis, Bactrocera psidii, Bactrocera tryoni, Bactrocera umbrosa, Bactrocera zonata, Ceratitis capitata, Ceratitis catoirii, Ceratitis quilicii, Dacus ciliatus, Dacus demmerezi, Neoceratitis cyanescens, and Zeugodacus cucurbitae. Manual curation allowed us to annotate 60-80 OR transcripts per species, including the obligatory coreceptor Orco. In total, we reported 698 new OR sequences. Differential expression analyses between antennae and maxillary palps and between the two sexes, performed in three species, revealed some organ- and sex-biased OR expression. Moreover, after adjusting for phylogenetic distance, we found significant correlations between some characteristics of the OR repertoire and species host range: sequences and relative expression level of several ORs were more conserved in polyphagous than in oligophagous species and, in addition, other ORs were found specifically in polyphagous species. Our results provide molecular insights into the ecological driving forces behind Tephritidae OR evolution.
昆虫嗅觉系统在引导物种找到特定的交配伙伴、不同的食物来源和产卵地点的过程中不断进化。负责检测挥发性信号的气味受体（OR）物种库是如何受到生态驱动力影响的，目前仍知之甚少。由于实蝇科（双翅目）的果蝇在其整个进化历史中经历了多次宿主转换，表现出高度多样化的宿主偏好，这使它们成为解决这个问题的良好模型。例如，对大量果蝇物种的基因组和转录组资源进行比较分析，可以得出统计学结论。在这里，我们采用RNA测序方法来鉴定13种具有不同宿主范围的实蝇科物种的OR库，这些物种分别是：弯背果实蝇、橘小实蝇、番石榴实蝇、昆士兰果实蝇、荫果实蝇、南瓜实蝇、地中海实蝇、卡氏果实蝇、奎氏果实蝇、具毛果实蝇、德氏果实蝇、蓝绿果实蝇和瓜实蝇。通过人工筛选，我们能够为每个物种注释60 - 80个OR转录本，包括必需的共受体Orco。我们总共报告了698条新的OR序列。在三个物种中进行的触角与下颚须之间以及两性之间的差异表达分析，揭示了一些器官和性别偏向的OR表达。此外，在校正系统发育距离后，我们发现OR库的一些特征与物种宿主范围之间存在显著相关性：几种OR的序列和相对表达水平在多食性物种中比在寡食性物种中更保守，此外，还发现其他OR仅存在于多食性物种中。我们的研究结果为实蝇科OR进化背后的生态驱动力提供了分子层面的见解。
