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.

The evolution of opsins and color vision: connecting genotype to a complex phenotype

“…In many systems it has been shown that opsin expression levels match the relative abundance of the different cone types leading to the conclusion that opsin expression reflects changes in relative cone abundances (Hagstrom et al, 1998). However, preliminary data suggest this might not be the case in birds (Bloch, 2015) and data is still not available for enough species, particularly beyond fish, to know whether opsin expression is generally a reflection of relative photoreceptor abundances (Fuller et al, 2004;Fuller and Claricoates, 2011).…”

“…In addition to variation in opsin gene sequence, opsin expression has been shown to vary significantly across species in various systems (Laver and Taylor, 2011;Sandkam et al, 2015), in many cases in a way consistent with variation in the light environment (Fuller et al, 2004;Hofmann et al, 2009;Fuller et al, 2010;Bloch, 2015) or even measures of sexual selection (Bloch, 2015). The immediate consequences of changes in gene expression remain poorly understood.…”

“…For example fish living in turbid waters, which are rich in longer wavelength, have generally lost their short-sensitive opsin genes, do not express them or have visual pigments shifted to match their light environments (Yokoyama et al, 1999;Terai et al, 2002;Sugawara et al, 2005;Seehausen et al, 2008;Hofmann et al, 2009). More recent research indicates selection from the light environment could also be driving the evolution of opsin expression in birds (Bloch, 2015).…”

Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari (Cacajao calvus)

“…Several recent studies in invertebrates and vertebrates have shown a link between colour vision and intraspecific signalling (e.g. [1][2][3][4]), but there has been relatively little work on mammals. In New World monkeys (NWMs), colour vision is highly variable, and a substantial body of research has investigated the ecological and evolutionary basis of this variation [5], which has implications for the acquisition of trichromacy in humans, apes and Old World monkeys (Catarrhini) [6].…”

Rethinking our assumptions about the evolution of bird song and other sexually dimorphic signals

“…Indeed, dimorphisms in both song and plumage colors have been shown to be associated with an assortment of life history traits besides mating system, including breeding latitude, seasonal migration, nesting behavior, and territoriality (Martin and Badyaev, 1996;Friedman et al, 2009;Price, 2009;Soler and Moreno, 2012;Johnson et al, 2013;Odom et al, 2015). Nevertheless, the perception that levels of sexual dimorphism reflect levels of sexual selection remains pervasive, even among some researchers (e.g., Seddon et al, 2013;Bloch, 2015).…”