Deep-sea and pelagic rod visual pigments identified in the mysticete whales

The New Jersey Center for Science, Technology & Mathematics, Kean University, Union, New Jersey, USA.
Visual Neuroscience (Impact Factor: 2.21). 03/2012; 29(2):95-103. DOI: 10.1017/S0952523812000107
Source: PubMed


Our current understanding of the spectral sensitivities of the mysticete whale rod-based visual pigments is based on two species, the gray whale (Eschrichtius robustus) and the humpback whale (Megaptera novaeangliae) possessing absorbance maxima determined from difference spectra to be 492 and 497 nm, respectively. These absorbance maxima values are blueshifted relative to those from typical terrestrial mammals (≈500 nm) but are redshifted when compared to those identified in the odontocetes (479-484 nm). Although these mysticete species represent two of the four mysticete families, they do not fully represent the mysticete whales in terms of foraging strategy and underwater photic environments where foraging occurs. In order to better understand the spectral sensitivities of the mysticete whale rod visual pigments, we have examined the rod opsin genes from 11 mysticete species and their associated amino acid substitutions. Based on the amino acids occurring at positions 83, 292, and 299 along with the directly determined dark spectra from expressed odontocete and mysticete rod visual pigments, we have determined that the majority of mysticete whales possess deep-sea and pelagic like rod visual pigments with absorbance maxima between 479 and 484 nm. Finally, we have defined the five amino acid substitution events that determine the resulting absorbance spectra and associated absorbance maxima for the mysticete whale rod visual pigments examined here.

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    • "The exceptions were Chelidonichthys kumu (292A/299A), and, as previous stated, N. celidotus (292S/299S). The combination 83 N/292A/299S was detected in the rhodopsin sequence of mysticete whales with a λ max value of 493 nm (Bischoff et al. 2012). Therefore, it is likely that the combination 292A/299S detected here in most of the epipelagic species is related to an adaptation to longer wavelengths of light in comparison with the deeper species. "
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    ABSTRACT: Critical amino acid replacements in opsin proteins shift the maximal absorbance of visual pigments to perceive different photic environments (spectral tuning). Here we studied the molecular basis for spectral tuning of the rhodopsin (RH1) pigment in 19 species of marine teleosts inhabiting different light environments, from shallow waters to the deep-sea. We identified replacements at the critical sites 194, 195, 292 and 299, which have been defined relative to the bovine RH1 gene and are known to be involved in shifting the λmax value of RH1 pigments towards the blue light. All the species had the substitutions P194R and H195A. However, we detected a relationship between the combination of amino acids at the critical sites 292 and 299 and the maximum depth of the species under study. The combination 292S/299A was only found in the deep-sea congeners Hoplostethus atlanticus and H. mediterraneus. This may reflects an adaptation of these species to the bathypelagic light environment. All the epipelagic species studied and the epi-mesopelgic species Parapercis colias, had the combination 292A/299S, except Chelidonichthys kumu (292A/299A) and Notolabrus celidotus (292S/299S). It is possible that the combination 292A/299S is an adaptation to longer wavelengths of light in comparison with the deeper species. This is the first study in the rhodopsin gene sequence in all the species under study, except for Macruronus novaezelandiae and H. mediterraneus.
    Environmental Biology of Fishes 11/2014; 98(1):193-200. DOI:10.1007/s10641-014-0249-4 · 1.57 Impact Factor
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    Proceedings of the Royal Society B: Biological Sciences 02/2013; 280(1753):20122645. DOI:10.1098/rspb.2012.2645 · 5.05 Impact Factor
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    ABSTRACT: Cetaceans have a long history of commitment to a fully aquatic lifestyle that extends back to the Eocene. Extant species have evolved a spectacular array of adaptations in conjunction with their deployment into a diverse array of aquatic habitats. Sensory systems are among those that have experienced radical transformations in the evolutionary history of this clade. In the case of vision, previous studies have demonstrated important changes in the genes encoding rod opsin (RH1), short-wavelength sensitive opsin 1 (SWS1), and long-wavelength sensitive opsin (LWS) in selected cetaceans, but have not examined the full complement of opsin genes across the complete range of cetacean families. Here, we report protein-coding sequences for RH1 and both color opsin genes (SWS1, LWS) from representatives of all extant cetacean families. We examine competing hypotheses pertaining to the timing of blue shifts in RH1 relative to SWS1 inactivation in the early history of Cetacea, and we test the hypothesis that some cetaceans are rod monochomats. Molecular evolutionary analyses contradict the "coastal" hypothesis, wherein SWS1 was pseudogenized in the common ancestor of Cetacea, and instead suggest that RH1 was blue-shifted in the common ancestor of Cetacea before SWS1 was independently knocked out in baleen whales (Mysticeti) and in toothed whales (Odontoceti). Further, molecular evidence implies that LWS was inactivated convergently on at least five occasions in Cetacea: (1) Balaenidae (bowhead and right whales), (2) Balaenopteroidea (rorquals plus gray whale), (3) Mesoplodon bidens (Sowerby's beaked whale), (4) Physeter macrocephalus (giant sperm whale), and (5) Kogia breviceps (pygmy sperm whale). All of these cetaceans are known to dive to depths of at least 100 m where the underwater light field is dim and dominated by blue light. The knockout of both SWS1 and LWS in multiple cetacean lineages renders these taxa rod monochromats, a condition previously unknown among mammalian species.
    PLoS Genetics 04/2013; 9(4):e1003432. DOI:10.1371/journal.pgen.1003432 · 7.53 Impact Factor
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