Massive parallel regression: a précis of genetic mechanisms for vision loss in diving beetles

Abstract

Two tribes of subterranean dytiscid diving beetles independently colonised groundwater systems of the Western Australian arid zone, a habitat transition that was most likely driven by the contraction of surface water bodies following late Neogene aridification of the Australian continent. These 'stygofauna' are now trapped within discrete calcrete aquifers that have formed in palaeodrainage valleys, resulting in the world's most diverse radiations of subterranean dytiscid beetles. Approximately 100 species from three genera exhibit partial or fully regressed visual systems and are essentially blind. This unique study system, with multiple independent transitions to subterranean life enables regressive and adaptive evolutionary processes to be studied in parallel at an unheralded comparative scale. Here we provide an overview of the progression of dytiscid beetle research and undertake a literature survey of published research within the field of regressive evolution as it applies to eye loss. We detail our exploration of insect vision genes for signatures of adaptive and neutral evolutionary mechanisms related to eye regression, largely within photoreceptor and eye pigment genes. Our project makes use of transcriptome data from five representative dytiscid beetle species (two surface and three subterranean) in order to design a customized set of RNA baits for use in a hybrid-capture method to target a pool of vision genes sequenced using high-throughput Illumina platforms. This methodological design permits the assessment of modifications in the genomic sequence of beetle vision genes at a much broader scale than Sanger sequencing, enabling a higher number of both target species and genes to be simultaneously assessed relative to research time-investments. Based on our literature search criteria of the research field ('regressive evolution' + 'eyes'), 81 papers have been published since the late 1980's accruing an h-index of 27 and a mean citation rate of 24.57. Collective annual citations for this field of research have surged over the past five years, an indication that broader scientific community interest is gaining momentum. The majority of publications (75%) have focused on the chordate clade Actinopterygii. Historically, research on variant subterranean taxa have faced difficulties inferring the evolutionary mechanisms of eye regression (and vision loss) using molecular approaches because only a handful of target genes could be feasibly addressed within grant funding cycles. From a comparative phylogenetic perspective, next-generation sequencing approaches applied to stygobiontic dytiscid beetles hold the potential to greatly improve our understanding of the genetic mechanisms underlying regressive evolution generally.