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.

Figure 1. A hypothesis for the evolution of LWS, SWS1, and RH1 in Cetacea and outgroups.

Phylogenetic relationships and divergence times for Cetacea follow McGowen et al. and for outgroups are as in Meredith et al. . Nodes in the tree are numbered (1–50) and are referenced to in the main text. The coloration of branches indicates inferred functional SWS1 (blue), functional LWS (red), and functional RH1 (black); for example, all three opsins are reconstructed as functional in the common ancestor of Cetacea (node 26 to node 27), but only RH1 is functional in balaenopteroid baleen whales (node 31 and its descendants). Inferred inactivation events (frameshifts, premature stop codons, etc.) are marked by yellow circles with Xs, and are arbitrarily placed at the midpoints of branches to which these events were optimized. Inferred red and blue shifts in λ_max for LWS and RH1 are indicated by arrows at internodes. Geological time scale is shown at the bottom of the figure with time in millions of years (Plio = Pliocene; P = Pleistocene). For taxon names, the mysticete genus Balaenoptera is abbreviated as “B.”. Paintings are by Carl Buell.