Abstract
Following gene duplication events, the expression patterns of the resulting gene copies can often diverge both spatially and temporally. Here we report on gene duplicates that are expressed in distinct but overlapping patterns, and which exhibit temporally divergent expression. Butterflies have sophisticated color vision and spectrally complex eyes, typically with three types of heterogeneous ommatidia. The eyes of the butterfly Papilio xuthus express two green- and one red-absorbing visual pigment, which came about via gene duplication events, in addition to one ultraviolet (UV)- and one blue-absorbing visual pigment. We localized mRNAs encoding opsins of these visual pigments in developing eye disks throughout the pupal stage. The mRNAs of the UV and blue opsin are expressed early in pupal development (pd), specifying the type of the ommatidium in which they appear. Red sensitive photoreceptors first express a green opsin mRNA, which is replaced later by the red opsin mRNA. Broadband photoreceptors (that coexpress the green and red opsins) first express the green opsin mRNA, later change to red opsin mRNA and finally re-express the green opsin mRNA in addition to the red mRNA. Such a unique temporal and spatial expression pattern of opsin mRNAs may reflect the evolution of visual pigments and provide clues toward understanding how the spectrally complex eyes of butterflies evolved.
Highlights
The structure and function of visual systems vary depending on animals’ habitats and foraging strategies
Compound eyes consist of thousands of ommatidia each housing several photoreceptor cells, with the precise number of photoreceptors differing among species (Figure 1; Friedrich et al, 2011; Wernet et al, 2015)
We studied the anatomy of developing compound eyes in Papilio xuthus with particular attention to the expression of opsin mRNAs in photoreceptor precursors
Summary
The structure and function of visual systems vary depending on animals’ habitats and foraging strategies. Compound eyes consist of thousands of ommatidia each housing several photoreceptor cells, with the precise number of photoreceptors differing among species (Figure 1; Friedrich et al, 2011; Wernet et al, 2015). The ommatidia can typically be divided into two or three spectrally distinct types according to the spectral sensitivities of their photoreceptors. Species with two ommatidial types in their main retina, such as locusts (Schmeling et al, 2014), leafhoppers (Wakakuwa et al, 2014), and flies (Franceschini et al, 1981; Chou et al, 1999) have eight photoreceptors (R1-8) in each ommatidium. Eye Development the ommatidia of butterflies and bees typically bear nine photoreceptor cells (R1-9), and their main retinas contain three types of ommatidia (Figures 1A,C)
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