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Elaboration and degeneration of complex traits: The visual systems of lizards and snakes

Periodic Reporting for period 1 - Evol-Eyes (Elaboration and degeneration of complex traits: The visual systems of lizards and snakes)

Reporting period: 2016-10-01 to 2018-09-30

How are complex traits lost during evolution, and once lost how can they be regained? Our project addresses these fundamental questions using the exceptionally diverse visual systems of squamate reptiles (snakes and lizards). Specialist nocturnal and burrowing lineages have evolved many times in squamates, offering multiple in- dependent comparisons of taxa that have lost genes in functionally redundant visual pathways. Two groups, snakes and geckos, lost several key visual genes during such ‘sensory bottlenecks’, but both show remarkable re-innovation of eye anatomy and physiology: diurnal snakes inherited incomplete cone (bright-light) photoreceptor and transduction pathways from their nocturnal/burrowing ancestors but have highly sensitive colour vision; geckos are descended from diurnal lizards and lack major components of the rod (low-light) pathway, but secondarily nocturnal species have superb night vision. We will use this powerful comparative framework to 1) thoroughly reconstruct patterns of reduction and loss of visual gene function in squamates that have entered low light environments, and 2) discover the molecular mechanisms that have compensated for ancestral gene losses in exemplar snake and gecko taxa with secondarily evolved visual capabilities. This will yield significant new knowledge of the fundamental processes of gene loss in evolution and provide a paradigmatic case of evolutionary re-innovation following degeneration in complex traits.
Work Package 1 – Exploring the Squamate Visual System [Near Completion]
Fieldwork was be carried out in South Australia, Western Australia Queensland for target species. During these fieldwork expeditions I collected lizards and snakes with the aim of covering most of ecological diversity and multiple lineages. Fieldwork was done under research permits issued by Australian State governments.
The retinal tissues for each of these lizard and snakes was removed, RNA extracted and sent to NGS sequencing. I currently have sequenced 36 squamate reptiles eye transcriptomes and waiting for transcriptome data for an additional 87 squamates.
Additionally, I collected microspectrophotometry data for 12 animals and electroretinography data for 8 Squamates through collaborators. Further 26 species were studied for retinal anatomy and photoreceptor complement under light and electronic microscopy methods.

1.2.2 Work package 2 – Expanding Taxon Selection [Near Completion]
I designed a gene-capture probes to sequence genes involved in visual sensory perception, circadian rhythm and genes involved in retinal degeneration (retinopathy diseases) in humans. I collected the samples from the ABTC collection in the South Australia Museum and across other Natural History Museums across the world. Sampling comprises 95% of all squamate lineages, diverse ecologies (nocturnal vs diurnal, subterranean vs above ground, terrestrial vs aquatic). I sequenced the visual genes for 96 species and I currently waiting for the visual gene data for further 480 species.

1.2.3 Work package 3: Phylogenomic, comparative genomic and transcriptomic analysis [Currently in progress]
My project will contribute substantially by combining gene sequence comparisons and expression data for all major visual pathways across multiple independent transitions, spanning recent to relatively ancient divergence timescales. Our multispecies approach will also provide significant empirical data to test model estimates of the timeframes that inactivated genes can lie latent without being irreversibly lost. I have generated substantial genetic data to study the visual system of lizard and snakes, produced data for eye anatomy and physiology. The data is currently being analysed and I'm currently writing some publications to submit to peer-review journals
Left: Dr Bruno Simões doing fieldwork in sea snakes; T-R: Gecko; B-R: Sleepy lizard