Transcriptome-wide expression variation associated with environmental plasticity and mating success in the cactophilic Drosophila mojavensis

Ecological speciation occurs with the adaptation of populations to different environments and concurrent evolution of reproductive isolation. The role of phenotypic plasticity might influence both ecological adaptation and reproductive traits. We examined environment-specific gene expression and male mating success in a cactophilic Drosophila using transcriptome sequencing. Drosophila mojavensis exhibits cactus-dependent mating success across different species of host plants, with genotype-by-environment interactions for numerous traits. We cultured flies from egg to eclosion on two natural cactus hosts and surveyed gene expression in adult males that were either successful or unsuccessful in achieving copulation in courtship trials. We identified gene expression differences which included functions involved with metabolism, most likely related to chemical differences between host cactus species. Several epigenetic related functions were identified that might play a role in modulating gene expression in adults due to host cactus effects on larvae. Cactus-dependent mating success implicated expression differences of genes involved in translation, transcription and nervous system development. This suggests a role of neurological function genes in the mating success of D. mojavensis males. Together, these results suggest that the influence of environmental variation on mating success via regulation of gene expression might be an important aspect of ecological speciation.

生态物种形成（ecological speciation）指种群适应不同环境的同时，生殖隔离同步演化的生物学过程。表型可塑性（phenotypic plasticity）可能同时对生态适应与生殖性状产生影响。本研究通过转录组测序（transcriptome sequencing）技术，针对嗜仙人掌果蝇（cactophilic Drosophila）的环境特异性基因表达模式与雄性交配成功率展开了探究。莫哈韦果蝇（Drosophila mojavensis）在不同宿主仙人掌物种上均表现出依赖仙人掌的交配成功率，且诸多性状存在基因型-环境互作（genotype-by-environment interactions）。我们将果蝇从卵期饲养至羽化阶段，所用基质为两种天然仙人掌，并对求偶试验中成功完成交配与未成功交配的成年雄性个体的基因表达水平进行了检测。本研究鉴定得到的基因表达差异涉及代谢相关功能，这大概率与不同宿主仙人掌物种间的化学组成差异相关。此外，我们还鉴定出若干表观遗传（epigenetic）相关功能模块，它们可能通过调控成年个体的基因表达，以响应宿主仙人掌对幼虫阶段的影响。依赖仙人掌的交配成功率与参与翻译、转录及神经系统发育的基因表达差异显著相关，这提示神经系统功能基因在莫哈韦果蝇雄性的交配成功过程中发挥了关键作用。综上，本研究结果表明，环境变异通过调控基因表达进而影响交配成功率，这一过程可能是生态物种形成的重要环节。