Daily activity patterns influence retinal morphology, signatures of selection, and spectral tuning of opsin genes in colubrid snakes

Autor(es)

Hauzman, E. ^{[1, 2]} ; Bonci, D. M. O. ^{[1, 2]} ; Suarez-Villota, E. Y. ^{[3, 4]} ; Neitz, M. ^[5] ; Ventura, D. F. ^{[1, 2]}

Afiliação do(s) autor(es)

^[1] Inst Israelita Ensino & Pesquisa Albert Einstein, Sao Paulo - Brazil

^[2] Univ Sao Paulo, Inst Psicol, Dept Psicol Expt, Av Prof Mello Moraes 1721 Bloco A Sala D9, BR-05508030 Sao Paulo, SP - Brazil

^[3] Inst Butantan, Lab Ecol & Evolucao, Sao Paulo - Brazil

^[4] Univ Austral Chile, Inst Ciencias Marinas & Limnol, Edificio Emilio Pugin, Campus Isl Teja S-N, Valdivia 5110236 - Chile

^[5] Univ Washington, Dept Opthalmol, 750 Republican St, Box 358058, Seattle, WA 98109 - USA

• Tipo de documento: Artigo Científico
• Fonte: BMC Evolutionary Biology; v. 17, DEC 11 2017.
• Citações Web of Science: 6

Resumo

Background: Morphological divergences of snake retinal structure point to complex evolutionary processes and adaptations. The Colubridae family has a remarkable variety of retinal structure that can range from all-cone and all-rod to duplex (cone/rod) retinas. To explore whether nocturnal versus diurnal activity is responsible for constraints on molecular evolution and plays a role in visual opsin spectral tuning of colubrids, we carried out molecular evolution analyses of the visual opsin genes LWS, RH1, and SWS1 from 17 species and performed morphological analyses. Results: Phylogenetic reconstructions of the RH1 and LWS recovered major clades characterized by primarily diurnal or primarily nocturnal activity patterns, in contrast with the topology for SWS1, which is very similar to the species tree. We found stronger signals of purifying selection along diurnal and nocturnal lineages for RH1 and SWS1, respectively. A blue-shift of the RH1 spectral peak is associated with diurnal habits. Spectral tuning of cone opsins did not differ among diurnal and nocturnal species. Retinas of nocturnal colubrids had many rows of photoreceptor nuclei, with large numbers of rods, labeled by wheat germ agglutinin (WGA), and two types of cones: large cones sensitive to long/medium wavelengths (L/M) and small cones sensitive to ultra-violet/violet wavelengths (UV/VS). In contrast, retinas of diurnal species had only one row of photoreceptor nuclei, with four types of cones: large and double L/M cones, small UV/VS cones, and a second group of small cones, labeled by WGA. Conclusions: For LWS gene, selection tests did not confirm different constraints related to activity pattern. For SWS1, stronger purifying selection in nocturnal lineages indicates divergent evolutionary pressures related to the activity pattern, and the importance of the short wavelength sensitivity at low light condition. Activity pattern has a clear influence on the signatures of selection and spectral tuning of RH1, with stronger purifying selection in diurnal lineages, which indicates selective pressure to preserve rhodopsin structure and function in pure-cone retinas. We suggest that the presence of four cone types in primarily diurnal colubrids might be related to the gain of color discrimination capacity. (AU)

• Processo FAPESP: 10/51670-8 - Ecologia e evolução do sistema visual de serpentes Caenophidia: estudos comparativos da morfologia retiniana e genética de opsinas
• Beneficiário: Einat Hauzman
• Linha de fomento: Bolsas no Brasil - Doutorado
• Processo FAPESP: 11/17423-6 - Estudo dos pigmentos visuais de primatas do Novo Mundo e análise de marcadores genéticos para retinopatia diabética
• Beneficiário: Daniela Maria Oliveira Bonci
• Linha de fomento: Bolsas no Brasil - Pós-Doutorado
• Processo FAPESP: 14/26818-2 - Desenvolvimento e implantação de métodos de avaliação visual: aplicações clínicas e em modelos animais
• Beneficiário: Dora Selma Fix Ventura
• Linha de fomento: Auxílio à Pesquisa - Temático
• Processo FAPESP: 09/06026-6 - Estudo psicofísico e genético das deficiências da visão de cores em humanos com diferentes patologias
• Beneficiário: Dora Selma Fix Ventura
• Linha de fomento: Auxílio à Pesquisa - Regular
• Processo FAPESP: 14/25743-9 - Expressão de opsinas e melanopsinas em retinas de serpentes: genética molecular e imunohistoquímica
• Beneficiário: Einat Hauzman
• Linha de fomento: Bolsas no Brasil - Pós-Doutorado
• Processo FAPESP: 08/58731-2 - A visão como indicador de processos lesivos na retina e no sistema nervoso central
• Beneficiário: Dora Selma Fix Ventura
• Linha de fomento: Auxílio à Pesquisa - Temático