Evolutionary history limits species' ability to match colour sensitivity to available habitat light

Abstract

The spectrum of light that an animal sees-from ultraviolet to far red light-is governed by the number and wavelength sensitivity of a family of retinal proteins called opsins. It has been hypothesized that the spectrum of light available in an environment influences the range of colours that a species has evolved to see. However, invertebrates and vertebrates use phylogenetically distinct opsins in their retinae, and it remains unclear whether these distinct opsins influence what animals see, or how they adapt to their light environments. Systematically using published visual sensitivity data from across animal phyla, we found that terrestrial animals are more sensitive to shorter and longer wavelengths of light than aquatic animals and that invertebrates are more sensitive to shorter wavelengths of light than vertebrates. Using phylogenetically controlled analyses, we found that closed and open canopy habitat species have different spectral sensitivities when comparing across the Metazoa and excluding habitat generalists, while deepwater animals are no more sensitive to shorter wavelengths of light than shallow-water animals. Our results suggest that animals do adapt to their light environment; however, the invertebrate-vertebrate evolutionary divergence may limit the degree to which animals can perform visual tuning.

Keywords: ciliary opsin; light environment; meta-analysis; rhabdomeric opsin; visual tuning; λmax.

Figure 1.

Our phylogeny of species used in the meta-regressions. Both chordates and non-chordates experienced transitions from aquatic to terrestrial environments, and terrestrial chordates experienced a return to aquatic environments from terrestrial environments. Silhouettes representing sampled Metazoan phyla, clockwise from top: jellyfish: cnidarians; elephant: chordates; squid: mollusks; butterfly: arthropods. (Online version in colour.)

Figure 2.

Effect of coarse habitat and lineage on mean visual pigment sensitivity. (a) Longest opsin: aquatic invertebrates: n = 78, µ = 503.3 nm; aquatic vertebrates: n = 273, µ = 507.6 nm; terrestrial invertebrates: n = 43, µ = 530.3 nm; terrestrial vertebrates: n = 39, µ = 539.1 nm. (b) Shortest opsin: aquatic invertebrates: n = 78, µ = 485.3 nm; aquatic vertebrates: n = 273 µ = 473.0 nm; terrestrial invertebrates: n = 43, µ = 430.1 nm; terrestrial vertebrates: n = 39, µ = 456.1 nm. (c) Opsin range: aquatic invertebrates: n = 78, µ = 18.0 nm; aquatic vertebrates: n = 273, µ = 34.6 nm; terrestrial invertebrates: n = 43, µ = 100.2 nm; terrestrial vertebrates: n = 39, µ = 83.0 nm. *p < 0.05. Analyses not controlled by phylogeny. (Online version in colour.)

Figure 3.

Effect of habitat greenness on visual sensitivities. (a) Longest opsin: forest + intermediate: n = 14, µ = 547.1 nm, s.d. = 17.71 nm; coastal: n = 40, µ = 297.3 nm, s.d. = 72.42 nm; freshwater: n = 23, µ = 314.3 nm, s.d. = 73.77 nm; open terrestrial: n = 22, µ = 534.1 nm, s.d. = 49.09 nm. (b) Shortest opsin: forest + intermediate: n = 14, µ = 470.4 nm, s.d. = 60.00 nm; coastal: n = 40, µ = 254.4 nm, s.d. = 55.16 nm; freshwater: n = 23, µ = 261.1 nm, s.d. = 56.52 nm; open terrestrial: n = 22, µ = 423.4 nm, s.d. = 82.06 nm. (c) Opsin range: forest + intermediate: n = 14, µ = 76.63 nm, s.d. = 72.61 nm; coastal: n = 40, µ = 742.88 nm, s.d. = 70.15 nm; freshwater: n = 23, µ = 53.26 nm, s.d. = 69.30 nm; open: n = 22, µ = 110.6 nm, s.d. = 98.82 nm. *p < 0.05. Analyses controlled for phylogeny. (Online version in colour.)