Role of the iridescent eye in stickleback female mate choice

Abstract

SUMMARYMany vertebrates exhibit prominent body colours that are used in courtship and territorial communication. Some fishes also have an eye whose iris becomes iridescent during the mating season, as in the threespine stickleback. Behavioural studies in this species have focused on the redness of the throat/jaw as the primary determinant of female mate choice. Unlike the iridescent eye, however, the red throat/jaw is not present in all stickleback populations, suggesting that the colour of the eye may be equally important for female mate choice. Here, we used data on photoreceptors and environmental light to assess body conspicuousness and the colour contrast of courtship signals for stickleback populations living in a range of waters, from clear (mesotrophic) to red light shifted (dystrophic). This analysis indicated that the redness of the throat/jaw is expressed to enhance the contrast of the eye. To test the importance of eye colour as a courtship signal, we carried out mate choice experiments in which females were presented with identical videos of a courting male but for the colour of the eye and/or the throat/jaw. Females did not choose based on differences in throat/jaw redness between videos, but preferred males with the highest contrast between the eye and the throat/jaw. This result points to the blue iridescent eye as a primary courtship signal in stickleback female mate choice.

Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments

“…Increased color contrast attention might also be favored by sexual selection: the “blue morph” in bluefin killifish is more abundant in blackwater, and blue males are preferred by individuals raised in stained water [63, 64]. Similarly, stickleback inhabiting blackwater systems have lost red nuptial throat color and instead show black throats, contrasting with the background and with blue eyes, and these two traits are under sexual selection by choosy females [17, 19]. Spectral tuning of blue-sensitive SWS2 may thus be under both natural and sexual selection in threespine stickleback and other blackwater-adapted fish species.…”

“…Not only natural selection by predators, but also sexual selection interacts with light spectra: blackwater stickleback males have replaced red with black nuptial throat color, which maximizes contrast to the blue eye and against the background via reversed counter-shading [17]. And both traits, the black throat and blue eyes, are preferred by females choosing their mates [19]. Also, color vision was adapted to the blackwater light spectrum: double cones in the retina of stickleback from blackwater systems express only red light–sensitive photopigments instead of one red and one green light–sensitive photopigment, increasing the stickleback’s visual sensitivity to dominant red light [18].…”

Regulation of eye and jaw colouration in three‐spined stickleback Gasterosteus aculeatus

“…Physiological colour change is modulated primarily by four hormones in fish: α‐melanocyte stimulating hormone (α‐MSH) mediates pigment dispersion, while melanin‐concentrating hormone (MCH), noradrenaline (NA) and melatonin (MEL) mediate pigment aggregation (Fujii, ; Aspengren et al, ; Bagnara & Matsumoto, ). Colour change in fish eyes is less investigated than colour change in skin, but it has recently been shown to be involved in social rank, reproduction and camouflage enhancement (Castro et al, ; Miyai et al, ; Flamarique et al, ; Freitas et al, ; Sköld et al, ). While both eye and skin chromatophores in the cryptic sand gobies respond to MCH and NA with pigment aggregation and to MSH and adrenocorticotropic hormone with pigment dispersion (Sköld et al, ), there is no information about eye colour regulation in species that use eye colour for signalling.…”

“…The red jaw colour is associated with higher offspring survival and disease resistance, thus providing a fitness indicator to choosy females (Barber et al ., ; Candolin & Tukiainen, ). While the red jaw colouration has received more attention (Malek et al, ), the blue eye colouration was recently shown to be important to attract females too (Flamarique et al, ). Flamarique et al .…”

“…Flamarique et al . () showed that females responded to videos of artificially coloured males, that females did not choose based on differences in jaw redness, but preferred males with the highest contrast between the eye and the jaw, indicating a need for a better understanding of G. aculeatus eye appearance. Both characteristics have adjustable colouration that rapidly increases or decreases in intensity within a few days during mating behaviour and are most intense during courtship (McLennan & McPhail, ).…”