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

Abstract

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 lwop indicated 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.

The transcriptomes of cave and surface populations of Gammarus minus (Crustacea: Amphipoda) provide evidence for positive selection on cave downregulated transcripts

“…Of the differentially regulated genes (> twofold change in expression), 71.7% exhibited decreased expression in the cave species. Similarly, significantly decreased expression levels of three different opsin transcripts were observed in multiple subterranean diving beetle species in comparison with related surface species [33]. We also observed significant decreases in the expression of visual genes in the subterranean population (discussed below), but the general trend toward upregulation in the cave population is difficult to explain.…”

Retinal perception and ecological significance of color vision in insects

“…Changes in Opsin number can be observed even within closely related species that prefer different light conditions, as shown by the comparisons between surface and subterranean species of predatory diving beetles [21*]. However, scorpionflies provide a conflicting example: common scorpionflies (Panorpidae) have somewhat colored bodies and wings but have lost two Opsins (SW and UV) with only one (LW) left, making them monochromats [59,69].…”

“…1C) [7**,18,19,20]. On the other hand, nocturnal insects have often lost Opsins or have reduced Opsin expression, which can affect an entire phylogenetic branch or just a single species [2,21*]. Some insects exhibit strategies to enhance color vision or regain previously lost sensitivities for certain wavelengths.…”

First Insights into the Subterranean Crustacean Bathynellacea Transcriptome: Transcriptionally Reduced Opsin Repertoire and Evidence of Conserved Homeostasis Regulatory Mechanisms

“…The authors suggested that loss of expression of opsin genes without loss of gene function is explained by the pleiotropic roles of opsin genes [36]. Extensive transcriptomic analysis revealed that three independently evolved subterranean diving beetles lack transcripts of nearly all opsin photoreceptor genes, whereas the two surface beetles showed evidence of transcriptional expression of a full suite of insect visual and non-visual opsin genes [47]. Thus, research on the absence or presence of putative opsin genes from the A .…”