Retention of duplicated long-wavelength opsins in mosquito lineages by positive selection and differential expression

Catherine A. Hill,Gloria I. Giraldo-Calderón,Michael J. Zanis

doi:10.1186/s12862-017-0910-6

Catherine A. Hill, Gloria I. Giraldo-Calderón + Show 1 more

Open Access

https://doi.org/10.1186/s12862-017-0910-6

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Abstract

BackgroundOpsins are light sensitive receptors associated with visual processes. Insects typically possess opsins that are stimulated by ultraviolet, short and long wavelength (LW) radiation. Six putative LW-sensitive opsins predicted in the yellow fever mosquito, Aedes aegypti and malaria mosquito, Anopheles gambiae, and eight in the southern house mosquito, Culex quinquefasciatus, suggest gene expansion in the Family Culicidae (mosquitoes) relative to other insects. Here we report the first detailed molecular and evolutionary analyses of LW opsins in three mosquito vectors, with a goal to understanding the molecular basis of opsin-mediated visual processes that could be exploited for mosquito control.ResultsTime of divergence estimates suggest that the mosquito LW opsins originated from 18 or 19 duplication events between 166.9/197.5 to 1.07/0.94 million years ago (MY) and that these likely occurred following the predicted divergence of the lineages Anophelinae and Culicinae 145–226 MY. Fitmodel analyses identified nine amino acid residues in the LW opsins that may be under positive selection. Of these, eight amino acids occur in the N and C termini and are shared among all three species, and one residue in TMIII was unique to culicine species. Alignment of 5′ non-coding regions revealed potential Conserved Non-coding Sequences (CNS) and transcription factor binding sites (TFBS) in seven pairs of LW opsin paralogs.ConclusionsOur analyses suggest opsin gene duplication and residues possibly associated with spectral tuning of LW-sensitive photoreceptors. We explore two mechanisms - positive selection and differential expression mediated by regulatory units in CNS – that may have contributed to the retention of LW opsin genes in Culicinae and Anophelinae. We discuss the evolution of mosquito LW opsins in the context of major Earth events and possible adaptation of mosquitoes to LW-dominated photo environments, and implications for mosquito control strategies based on disrupting vision-mediated behaviors.

Highlights

Opsins are light sensitive receptors associated with visual processes
Our results suggest that the 20 long wavelength (LW) opsins arose via multiple gene duplication events in the most recent common ancestor (MRCA) of the Anophelinae and Culicinae lineage in the Jurassic, approximately 197.5–166.9 million years ago (MY), following which independent duplications occurred at least once in each of the three mosquito lineages
The modest number of residues identified only in the most recently duplicated LW opsins likely reflects the stringency of FitModel. These residues are located in the 5′ extracellular and 3′ intracellular regions and TMDIII. While further work such as site-directed mutagenesis studies are required to determine the significance of this finding, and to evaluate a possible association between Trans-membrane domain (TMD) residues (C126 in CqGPRop5, 6 and AaGPRop2) and opsin spectral tuning, these analyses suggest that functional diversification may play a role in retention of at least some LW opsins in mosquitoes

Summary

Introduction

Opsins are light sensitive receptors associated with visual processes. Insects typically possess opsins that are stimulated by ultraviolet, short and long wavelength (LW) radiation. Six putative LW-sensitive opsins predicted in the yellow fever mosquito, Aedes aegypti and malaria mosquito, Anopheles gambiae, and eight in the southern house mosquito, Culex quinquefasciatus, suggest gene expansion in the Family Culicidae (mosquitoes) relative to other insects. Insects typically possess three classes of visual opsins that are sensitive to ultraviolet (UV, λmax 300–400 nm), short (SW, λmax 400–500 nm) and long (LW, λmax 500–600 nm) wavelengths. Non visual opsins have been identified and include the Apis mellifera (honey bee) pteropsin identified in the bee brain, suggesting a possible function in extra-retinal detection of light and the regulation of circadian rhythm [6,7,8,9]. The functions of the Drosophila melanogaster (fruit fly) opsin Rh7 [10] and the RGR-like and arthropsins identified in Daphnia pulex (common water flea) have not been determined

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