Roses, shopping trips, diamond earrings…lonely hearts go to great lengths to impress that special someone. Male animals make similar efforts to woo bachelorettes with dramatic markings and extravagant feathers. For her part, the bachelorette filters these signals through her eyes, and makes a decision based on what she perceives. A recent paper in PNAS from a trio of researchers from Tohoku University and the University of Tokyo, Japan, investigated how genetics and rearing environment shape the visual system of female guppies and whether that variation influences which future Mr Guppy she likes best.

Colour vision relies on opsin proteins in cone cells in the retina, and each opsin reacts to certain wavelengths (colours) of light. Always flamboyant, guppies sport nine opsin genes including red-sensitive opsins (LWS-1 and LWS-2) and green- or blue-sensitive opsins (SWS-1, SWS2-A, SWS2-B, and RH2-2). Variation in the amino acid sequences of each opsin influences its sensitivity to different coloured light: for example, if you replace the alanine amino acid at residue 180 in the guppy red LWS-1 opsin (‘Ala-type’) with a serine amino acid (‘Ser-type’), the opsin becomes sensitive to deeper shades of red. The team suspected that genetics and environmental changes could fine-tune guppy colour vision, and that this could shape the dating habits of female guppies.

First, Yusuke Sakai and colleagues compared how the genes that encode the different opsin proteins are converted into mRNA, a key step in the process where genes are eventually decoded to produce proteins; in this case, the opsins in the retina. The team compared mRNA production from the two forms of the LWS-1 opsin gene – Ala-type and Ser-type – in fish reared under white, green or orange light. They found that the Ser-type fish produced more red- and blue-sensitive opsin mRNAs. This suggests that Ser-type guppies pack more opsins into their eyes and may discriminate better between different colours. Regardless of which type of LWS-1 opsin the fish were producing, guppies that were raised in green or orange light produced less mRNA encoding UV- and blue-tuned opsins, probably because these opsins are not used as much in orange and green environments. So, guppies can alter how they express genes in response to the prevailing colour scheme in their environments.

However, gene expression data can be misleading because not every piece of mRNA gets involved in protein synthesis. The researchers then tested which opsin proteins were being produced from the mRNAs in the fish's eyes by testing how well each fish tracked moving visual patterns of orange or green light. Guppies with Ser-type LWS-1 opsin benefited from their opsin-packed eyes and tracked the moving visual patterns better than fish that had the Ala-type opsin. However, when fish reared under orange or green light were tested, the Ser-type fish lost their clear advantage. More opsin mRNA does lead to better colour vision, but only in some environments.

Having linked changes in opsin proteins to differences in colour vision, the team wanted to know how this influences what ‘she’ looks for in a husband. They had female guppies choose between two digitally modified videos of a male guppy: one with a big, sexy, ‘high orange (HO)’ marking and the other with a small, dull, ‘low orange (LO)’ marking. The females with more red- and blue-sensitive opsin mRNAs spent much more time near Mr HO than Mr LO. In other words, the females with extra opsins and good colour vision, loved their eye candy and found brightly coloured males more attractive than dull-coloured males.

Miss Guppy's genetics and rearing environment shape her colour vision and this relationship between visual physiology and mate preference may drive the evolution of extreme colouration in gentlemen guppies. For guppies, beauty is in the eye of the beholder and ladies with good eyes want bright orange eye candy.

Genetic and plastic variation in opsin gene expression, light sensitivity, and female response to visual signals in the guppy
Proc. Natl. Acad. Sci. USA.