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. 2014 May 6;6(6):1254-65.
doi: 10.1093/gbe/evu095.

Massive losses of taste receptor genes in toothed and baleen whales

Ping Feng  1 , Jinsong Zheng  2 , Stephen J Rossiter  3 , Ding Wang  2 , Huabin Zhao  4
Affiliations

Massive losses of taste receptor genes in toothed and baleen whales

Ping Feng et al. Genome Biol Evol. .

Abstract

Taste receptor genes are functionally important in animals, with a surprising exception in the bottlenose dolphin, which shows extensive losses of sweet, umami, and bitter taste receptor genes. To examine the generality of taste gene loss, we examined seven toothed whales and five baleen whales and sequenced the complete repertoire of three sweet/umami (T1Rs) and ten bitter (T2Rs) taste receptor genes. We found all amplified T1Rs and T2Rs to be pseudogenes in all 12 whales, with a shared premature stop codon in 10 of the 13 genes, which demonstrated massive losses of taste receptor genes in the common ancestor of whales. Furthermore, we analyzed three genome sequences from two toothed whales and one baleen whale and found that the sour taste marker gene Pkd2l1 is a pseudogene, whereas the candidate salty taste receptor genes are intact and putatively functional. Additionally, we examined three genes that are responsible for taste signal transduction and found the relaxation of functional constraints on taste signaling pathways along the ancestral branch leading to whales. Together, our results strongly suggest extensive losses of sweet, umami, bitter, and sour tastes in whales, and the relaxation of taste function most likely arose in the common ancestor of whales between 36 and 53 Ma. Therefore, whales represent the first animal group to lack four of five primary tastes, probably driven by the marine environment with high concentration of sodium, the feeding behavior of swallowing prey whole, and the dietary switch from plants to meat in the whale ancestor.

Keywords: diet; evolution; pseudogenization; taste receptor; whales.

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Figures

F<sc>ig</sc>. 1.—
Fig. 1.—
The species tree of whales with common mutations of T1Rs and T2Rs. The tree topology and divergence dates follow previous studies (Hasegawa et al. 2003; McGowen et al. 2009). Branch lengths are not drawn to scale; the numbers at the nodes are the divergence times in millions of years. T1R1 and T1R3 encode the umami taste receptor, T1R2 and T1R3 encode sweet taste receptors, and T2Rs confer bitter taste. For each gene, shared frame-shifting indels or premature stop codons across toothed and baleen whales are indicated by “S,” shared frame-shifting mutations in one of the two major lineages of whales are indicated with “S*” (toothed whales) or “S#” (baleen whales), and unshared ones are shown with “U.” Additionally, “+” indicates the presence of an intact ORF, “−” denotes the absence from the genome, while no signs in any gene indicate no amplifications despite numerous attempts.
F<sc>ig</sc>. 2.—
Fig. 2.—
An alignment of Pkd2l1 containing the ORF-disrupting mutations in two toothed whales (bottlenose dolphin and Yangtze River dolphin), one baleen whale (mink whale), and the outgroup (mouse). Codons in the correct reading frame are indicated by shading, and premature stop codons are boxed; the numbers in parentheses indicate the nucleotide positions following the mouse sequence.
F<sc>ig</sc>. 3.—
Fig. 3.—
An alignment of Calhm1 containing the ORF-disrupting mutations in seven toothed whales and four baleen whales. Dashes indicate alignment gaps, and question marks represent unamplified nucleotides. Codons in the correct reading frame are indicated by shading, whereas codons containing one nucleotide deletion or insertion are boxed.
F<sc>ig</sc>. 4.—
Fig. 4.—
The ML tree of Calhm1 in mammals under the GTR+I+G substitution model of sequence evolution. Branch lengths are drawn to scale. ML bootstrap values/Bayesian posterior probabilities (>50%) are shown as numbers above the branches.
F<sc>ig</sc>. 5.—
Fig. 5.—
An alignment of Trpm5 containing the ORF-disrupting mutations in two toothed whales (bottlenose dolphin and Yangtze River dolphin), one baleen whale (mink whale), and the outgroup (mouse).
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