Opsin transcripts of predatory diving beetles: a comparison of surface and subterranean photic niches

The regressive evolution of eyes has long intrigued biologists yet the genetic underpinnings remain opaque. A system of discrete aquifers in arid Australia provides a powerful comparative means to explore trait regression at the genomic level. Multiple surface ancestors from two tribes of diving beetles (Dytiscidae) repeatedly invaded these calcrete aquifers and convergently evolved eye-less phenotypes. We use this system to assess transcription of opsin photoreceptor genes among the transcriptomes of two surface and three subterranean dytiscid species and test whether these genes have evolved under neutral predictions. Transcripts for UV,long-wavelength and ciliary-type opsins were identified from the surface beetle transcriptomes. Two subterranean beetles showed parallel loss of all opsin transcription, as expected under ‘neutral’ regressive evolution. The third species Limbodessus palmulaoides retained transcription of a long-wavelength opsin (lwop) orthologue, albeit in an aphotic environment. Tests of selection on lwopindicated no significant differences between transcripts derived from surface and subterranean habitats, with strong evidence for purifying selection acting on L. palmulaoides lwop. Retention of sequence integrity and the lack of evidence for neutral evolution raise the question of whether we have identified a novel pleiotropic role for lwop, or an incipient phase of pseudogene development.

眼睛的退行性演化长期以来一直困扰着生物学家，但其遗传基础仍不明确。澳大利亚干旱地区的离散含水层系统为在基因组层面探究性状退行提供了强有力的比较研究手段。隶属于龙虱科（Dytiscidae）两个族的多个地表祖先类群多次入侵这些钙结层含水层，并趋同演化出无眼表型。本研究依托该系统，对2种地表龙虱与3种地下龙虱的转录组中的视蛋白感光基因（opsin photoreceptor genes）转录水平进行评估，并检验这些基因是否遵循中性演化预测的模式发生演化。研究人员从地表龙虱的转录组中成功鉴定出紫外（UV）、长波长以及纤毛型视蛋白的转录本。正如“中性”退行性演化理论的预测，2种地下龙虱均出现了所有视蛋白转录本完全丢失的平行演化特征。第三种物种掌肢新龙虱（Limbodessus palmulaoides）虽生存于无光环境中，却仍保留了长波长视蛋白（lwop）同源基因的转录活性。对lwop基因的选择压力检测结果显示，地表与地下生境来源的转录本之间无显著差异，且有充分证据表明掌肢新龙虱的lwop基因受到纯化选择作用。该基因序列完整性得以保留，且无中性演化的相关证据，这引发了一个新的问题：我们是否发现了lwop基因的全新多效性功能，抑或是该基因正处于假基因演化的初期阶段？