Opsins have evolved under the permanent heterozygote model: insights from phylotranscriptomics of Odonata

Abstract

Gene duplication plays a central role in adaptation to novel environments by providing new genetic material for functional divergence and evolution of biological complexity. Several evolutionary models have been proposed for gene duplication to explain how new gene copies are preserved by natural selection, but these models have rarely been tested using empirical data. Opsin proteins, when combined with a chromophore, form a photopigment that is responsible for the absorption of light, the first step in the phototransduction cascade. Adaptive gene duplications have occurred many times within the animal opsins' gene family, leading to novel wavelength sensitivities. Consequently, opsins are an attractive choice for the study of gene duplication evolutionary models. Odonata (dragonflies and damselflies) have the largest opsin repertoire of any insect currently known. Additionally, there is tremendous variation in opsin copy number between species, particularly in the long-wavelength-sensitive (LWS) class. Using comprehensive phylotranscriptomic and statistical approaches, we tested various evolutionary models of gene duplication. Our results suggest that both the blue-sensitive (BS) and LWS opsin classes were subjected to strong positive selection that greatly weakens after multiple duplication events, a pattern that is consistent with the permanent heterozygote model. Due to the immense interspecific variation and duplicability potential of opsin genes among odonates, they represent a unique model system to test hypotheses regarding opsin gene duplication and diversification at the molecular level.

Signatures of local adaptation along environmental gradients in a range‐expanding damselfly (Ischnura elegans)

“…Although weaker than for V‐ATPase, we detected a strong selection signature for long‐wavelength‐sensitive (LWS) opsin (annotated to SNP 73426_72; Table , Figure ), which is a phylogenetically diverse class of opsins in Odonata (Suvorov et al., ) that have previously been identified in transcriptomic analyses of I. elegans in Chauhan et al. (, ).…”

Retinal perception and ecological significance of color vision in insects

“…These polymorphisms might instead provide other physiological adaptations, such as the rate or cost of regeneration of the active photopigment, its expression level or (thermo)stability over time. This might enhance fitness in order to adapt to distinct environmental challenges without a change in spectral discrimination and explain the evolution and maintenance of additional diversity in a single species or the small changes between Opsins of closely related species [19,71**]. …”

“…For instance, Lepidoptera and dragonflies – usually regarded as having superior color vision – manifest a large number of Opsins and a high spectral diversity of photoreceptors (Fig. 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*].…”

Evolutionary ecology of opsin gene sequence, expression and repertoire

“…Lastly, Suvorov et al . () study an expansive opsin repertoire in the insect order Odonata and find evidence that copy number expansion is consistent with the permanent heterozygote model of gene duplication. Together these studies emphasize the utility of opsin genes for studying both the local adaptation of sensory systems and, more generally, gene family evolution.…”

“…The third study by Suvorov et al . () explores the evolutionary model behind a remarkable case of opsin gene repertoire expansion. Although fish are known for having some of the largest opsin repertoires among vertebrates, odonates (dragonflies and damselflies) have even larger opsin copy numbers, up to 30 genes (Futahashi et al .…”