Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins

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.

Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution

“…Three species-Odobenus rosmarus (walrus), Callorhinus ursinus (northern fur seal), Notoryctes typhlops (marsupial mole)-have intact coding sequences for complete or partial SWS1, but external evidence suggests that SWS1 cones are absent in each [68][69][70]. Our combined dataset describes 270 species with functional SWS1 cones, 214 of which have measured or predicted spectral tuning (electronic supplementary material, table S1), and 133 with nonfunctional SWS1 cones, a common trait in species occupying scotopic niches (see [2,12,17,49,54,[69][70][71] for discussion). Our novel sequence data increase the taxonomic coverage of SWS1 spectral tuning to 39 additional mammalian families.…”

“…presence/absence and/or spectral tuning), and added mammalian species and tetrapod outgroups from Meredith et al [53] to provide a robust backbone for the tree. We only included one representative from each cetacean family due to the parallel inactivation of SWS1 in odontocetes and mysticetes [54]. Some taxa with high percentages of missing gene sequences and/or non-overlapping sequences (e.g.…”

Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle

“…We noted that the expression of opsin genes displays significant differences between the pelagic and benthic stages. The expression levels of rod pigment (rh1) and cone pigment (lws1, also called opn1lw1) genes, which are responsible for scotopic vision and long-wavelength sensitivity 27 , respectively, are significantly higher in the benthic stages (P < 0.01), whereas the expression of the middle wavelength-sensitive pigment gene (rh2) was significantly higher in the pelagic stages (P < 0.01) (Supplementary Fig. 14 and Supplementary Table 20).…”

Farbensehen der Tiere

“…Alle Wale und Robben haben im Laufe der Evolution ihre SWS1-Zapfen als Anpassung an die sekundär aquatische Lebensweise verloren [25,[27][28][29][30][31]. Einige Arten der Bartenwale haben sogar eine reine Stäbchenretina [32]. Trotzdem berichten einzelne Verhaltensstudien mit Seebären, Seelöwen, Seehunden oder einem Delfin, diese marinen Säuger könnten Farben sehen [33,34] …”