Pelaez Julianne N, Gloss Andrew D, Goldman-Huertas Benjamin, Kim Bernard, Lapoint Richard T, Pimentel-Solorio Giovani, Verster Kirsten I, Aguilar Jessica M, Dittrich Anna C Nelson, Singhal Malvika, Suzuki Hiromu C, Matsunaga Teruyuki, Armstrong Ellie E, Charboneau Joseph L M, Groen Simon C, Hembry David H, Ochoa Christopher J, O'Connor Timothy K, Prost Stefan, Zaaijer Sophie, Nabity Paul D, Wang Jiarui, Rodas Esteban, Liang Irene, Whiteman Noah K
Department of Integrative Biology, University of California-Berkeley, Berkeley, CA 94720, USA.
Department of Biology, Brandeis University, Waltham, MA 02453, USA.
bioRxiv. 2023 Mar 16:2023.03.16.532987. doi: 10.1101/2023.03.16.532987.
Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genetic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families - genes directly mediating interactions with plant chemical defenses - underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many lineages are ancient (>150 million years ago [mya]), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across a genus nested within that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several non-herbivorous species. Comparative genomic analyses revealed that herbivorous have among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on plants (bitter or electrophilic phytotoxins) or their ancestral diet (yeast and fruit volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight strong gene candidates that have also been linked to other dietary transitions in .
食草昆虫种类异常多样，占所有已知真核生物物种的四分之一，但促成这种饮食转变的适应的遗传基础仍知之甚少。许多研究表明，化学感应和解毒基因家族的扩张和收缩——直接介导与植物化学防御相互作用的基因——是成功定殖植物的基础。然而，这一假设一直难以验证，因为许多谱系中的食草起源很古老（>1.5亿年前），掩盖了基因组进化模式。在这里，我们对一个属内的化学感应和解毒基因家族进化进行了表征，该属包括芥菜（十字花目）专家和石竹（石竹科）专家最近衍生的（<1500万年前）食草动物谱系，以及几个非食草物种。比较基因组分析表明，在所调查的12种果蝇物种中，食草果蝇的化学感应和解毒基因库最小。在超过一半的被调查基因家族中，食草动物分支的平均基因周转率显著高于背景率。然而，沿着祖先食草动物分支，基因周转率更为有限，只有味觉受体和气味结合蛋白经历了强烈的损失。受基因丢失、复制或选择约束变化影响最显著的基因是那些参与检测与以植物为食相关的化合物（苦味或亲电植物毒素）或其祖先饮食（酵母和水果挥发物）的基因。这些结果为植物取食适应的分子和进化机制提供了见解，并突出了与果蝇其他饮食转变也有关联的强大基因候选者。
