Evolution of opsin expression in birds driven by sexual selection and habitat

Abstract

Theories of sexual and natural selection predict coevolution of visual perception with conspecific colour and/or the light environment animals occupy. One way to test these theories is to focus on the visual system, which can be achieved by studying the opsin-based visual pigments that mediate vision. Birds vary greatly in colour, but opsin gene coding sequences and associated visual pigment spectral sensitivities are known to be rather invariant across birds. Here, I studied expression of the four cone opsin genes (Lws, Rh2, Sws2 and Sws1) in 16 species of New World warblers (Parulidae). I found levels of opsin expression vary both across species and between the sexes. Across species, female, but not male Sws2 expression is associated with an index of sexual selection, plumage dichromatism. This fits predictions of classic sexual selection models, in which the sensory system changes in females, presumably impacting female preference, and co-evolves with male plumage. Expression of the opsins at the extremes of the light spectrum, Lws and Uvs, correlates with the inferred light environment occupied by the different species. Unlike opsin spectral tuning, regulation of opsin gene expression allows for fast adaptive evolution of the visual system in response to natural and sexual selection, and in particular, sex-specific selection pressures.

Keywords: bird vision; opsin expression; sexual dimorphism.

Figure 1.

Male versus female normalized expression for (a) Uvs (b) Sws2 (c) Rh2 and (d) Lws. Opsin initial fluorescence (R₀) was used as a proxy for expression and normalized to an endogenous control, β-actin, as (see the electronic supplementary material for additional information). Each point corresponds to each species mean male and female expression. Note differences in axis scales. Grey 1 : 1 lines correspond to male = female expression, thus any species above the line have higher expression in females than males, and species below the line have higher male expression. Intraspecific variation and mean values can be found in the electronic supplementary material, figure S1 and table S1. (Online version in colour.)

Figure 2.

Relationship between Sws2 expression and sexual dimorphism in plumage in (a) females, y = 14.50x + 3.43 (phylogenetically corrected p < 0.0001) and (b) males, y = −3.45x + 4.73 (phylogenetically corrected p = 0.52). Species names are abbreviated as the first letter of the genus and the three first letters of the species. See Methods for full species names. Bird illustrations: male and female of Seiurus aurocapilla, a species sexually monomorphic for plumage (left) and Setophaga caerulescens (right). These are the species with the least and most sexually dichromatic plumage in the study. (Online version in colour.)

Figure 3.

Lws expression is higher in darker forest habitats than in brighter open and shrub habitats. Distribution of Lws relative expression values for males (grey) and females (white) of species occupying various habitats (N = 16 species). Boxes correspond to the first and third quartiles (the 25th and 75th percentiles). Whiskers extend to the lower and higher values and lines indicate the median. Points beyond the inter-quartile range are outliers. Habitat classifications for each species can be found in the electronic supplementary material, table S7.

Figure 4.

Uvs relative expression increases with habitat height. (a) Distribution of Uvs relative expression values for males (grey) and females (white) of species occupying ground (less than 1 m) and arboreal habitats. Boxes correspond to the first and third quartiles (the 25th and 75th percentiles). Whiskers extend to the lower and higher values and lines indicate the median. One outlier for each sex not shown (N = 15 species). Habitat classifications for each species can be found in the electronic supplementary material. See the electronic supplementary material, figure S5, for similar trend with a continuous classification of foraging height. (b) Irradiance as a function of wavelength for forest ground and tree canopy adapted from [44], illustrating how the lower habitats in the forests are relatively deprived of short-wavelengths.