Into the blue: Gene duplication and loss underlie color vision adaptations in a deep-sea chimaera, the elephant sharkCallorhinchus milii

Abstract

The cartilaginous fishes reside at the base of the gnathostome lineage as the oldest extant group of jawed vertebrates. Recently, the genome of the elephant shark, Callorhinchus milii, a chimaerid holocephalan, has been sequenced and therefore becomes the first cartilaginous fish to be analyzed in this way. The chimaeras have been largely neglected and very little is known about the visual systems of these fishes. By searching the elephant shark genome, we have identified gene fragments encoding a rod visual pigment, Rh1, and three cone visual pigments, the middle wavelength-sensitive or Rh2 pigment, and two isoforms of the long wavelength-sensitive or LWS pigment, LWS1 and LWS2, but no evidence for the two short wavelength-sensitive cone classes, SWS1 and SWS2. Expression of these genes in the retina was confirmed by RT-PCR. Full-length coding sequences were used for in vitro expression and gave the following peak absorbances: Rh1 496 nm, Rh2 442 nm, LWS1 499 nm, and LWS2 548 nm. Unusually, therefore, for a deep-sea fish, the elephant shark possesses cone pigments and the potential for trichromacy. Compared with other vertebrates, the elephant shark Rh2 and LWS1 pigments are the shortest wavelength-shifted pigments of their respective classes known to date. The mechanisms for this are discussed and we provide experimental evidence that the elephant shark LWS1 pigment uses a novel tuning mechanism to achieve the short wavelength shift to 499 nm, which inactivates the chloride-binding site. Our findings have important implications for the present knowledge of color vision evolution in early vertebrates.

Three cone opsin genes determine the properties of the visual spectra in the Japanese anchovy Engraulis japonicus (Engraulidae, Teleostei)

“…In EJ-LWS, these sites were occupied by AHYTA residues and the predicted λ max was 553nm, longer than our measurement. Davies et al (Davies et al, 2009;Davies et al, 2012) reported that the λ max value of elephant shark Callorhinchus milii LWS1 (EF565165) expressed in an in vitro experiment was not consistent with the 'five-site' rule, because of inactivation of the chloride ion positive charge of H197 caused by amino acid substitution of A308S. The EJ-LWS has amino acid residues H and A at sites 197 and 308 and our present knowledge could not explain the molecular mechanisms involved in the blue shift.…”

The evolution of early vertebrate photoreceptors

“…Therefore, it may be that at the time in evolutionary history when the jawed and jawless vertebrates split into two lineages, the eyes of lampreys possessed a predominantly photopic visual system based on cone-like photoreceptors. However, at least one type of receptor was undergoing some sort of 'transmutation' to a receptor hybrid, which would subsequently become a 'true rod' with the age of cartilaginous fishes (Walls 1942;Pisani et al 2006;Davies et al 2009). …”

“…In vertebrates, molecular phylogenetic analyses have established that vertebrate visual pigments evolved along five distinct lines and that these lineages may have been in place before the divergence of jawed and jawless fishes (Davies et al 2009; figure 2). The five vertebrate visual pigment gene lineages presumably diverged from a single common ancestor that had evolved prior to the divergence of the protostomes and deuterostomes, which is thought to have occurred about 700 Ma (Oota & Saitou 1999).…”

“…Until behavioural experiments are carried out, it will be difficult to understand the functional existence of up to three cone types and the potential for trichromatic colour vision in rays and elephant sharks (Hart et al 2006a,b;Davies et al 2009; figure 4d ). Most elasmobranchs display some degree of countershading, which tends to be most apparent in active, pelagic sharks, such as the blue shark, Review.…”

Identification and characterization of visual pigments in caecilians (Amphibia: Gymnophiona), an order of limbless vertebrates with rudimentary eyes

“…It is widely assumed that variations in the peak spectral sensitivities (l max ) of the visual system represent adaptations to specific visual needs associated with particular habitats or lifestyles (Lythgoe, 1979;Peichl, 2005;Davies et al, 2009). Spectral sensitivity is determined either by changes in the tertiary structure of the opsin protein via amino acid substitutions and/or by the use of alternate chromophores derived from vitamin A1 or A2 (Crescitelli et al, 1972;Yokoyama, 2000;Bowmaker and Hunt, 2006;Hart and Hunt, 2007).…”