R differences caused by achange indiet? that humans can, but there are exceptions. Are the Many vertebrates candetect the same five basic appetites lost The colleagues Edmund Ford and Julian Huxley bitter and others can’t . Fisher and his (PTC) that some humans nauseatingly find phenylthiocarbamidewith a chemical called ing chimps whether could taste water laced and spat at him. BY EWENCALLAWAY S16 | NATURE | S16 2012 VOL | JUNE 486|21 OUTLOOK EVOLUTIONARY BIOLOGY It was August 1939, and Fisher was test took asip of water, looked him eye in the achimpanzeewhen at Edinburgh Zoo onald Fisher must have relieved been TASTE -

it would at present useless to be conjecture,” the “Whereinspecies. advantages selective the lie, tion had maintained this diversity in both humans and chimps, and that natural selec caused by agenetic mutation shared by variation insensitivity to bitter tastes was with PTC. Fisher’s team speculated that the testedthey expressed their displeasure experiment pointless. make their preferences known, rendering the worried thathad been apesthe wouldn’t © 2012 Macmillan Publishers Limited. Allrights reserved Instead, about three-quarters of chimps the -

the usefulness of vision, the fish collected so cave-dwelling Alife fish. of darkness eliminated sylvania, likens situation the to that of sight in Center Philadelphia, in Penn Senses Chemical Beauchamp,Gary ageneticist at Monell the destroy ability their to make aworking protein. are liable to build up random mutations that not aid an animal’s or reproduction survival a game of ‘use it or it’, lose and that do chemicals Evolution certain infood. sense is history,ary ashiftindiet removed to need the changes is lifestyle. At some point inevolution of taste.” loss of evolution the really is taste of evolution ards and snakes, of whole story says: the “The Storrs studies who chemical sensing inliz biologist at the University of Connecticut in evolutionary benefit at Kurt all. Schwenk, a that, for many creatures, some tastes have no insight, culminating startlingdiscovery inthe ent animal genomes has given scientists more to figure it out.trying The availability of differ wrote trio irrelevant. However, applies theory this only to whole, food their moderating intake their is posits that dolphins because theory swallow in proteins) and bitter taste receptors. One working umami amino (which sense acids tors, dolphins lack ability the also to build dispensable.so As well as lacking sweet recep ing sweet receptor. Carnivora, bear, spectacled the has awork still team’s finding that an omnivorous member of says. This interpretation is supported by the tors switched to ameat-only diet,Beauchamp tions appeared after or each species its ances coursethe of evolution. Presumably muta the taste sweetness lost repeatedly had been over unique mutations, suggesting that ability the to in 7of them crippling mutations in thesweet-receptor sea-lions, otters and hyenas, and identified belonging to order the Carnivora, including spread. analysed 12non-feline They species inabilitythe to taste sweetness is more wide negating for need the a sweet receptor. of protein-rich meat, devoid plants,of sugary this ancestral animal moved to a diet composed that speculates Beauchamp ancestor. tionary gene inactive became common intheir evolu mutation, it is likely that the sweet-receptor domestic cats to lions —have an identical ofpart body. the felines all —from Because forwhether tongue, the intestine or any other genes that build aworking sweet receptor, share amutation that disables one of two the 2005 his found team finally out why champ noticed this quirk in 1970s, the and in home: cats cannot taste sweet substances. Beau ment and eventually lost sight their altogether. mutations in genes involved in eye develop The most obvious explanation for the More than 70years later, biologists are still There may other be reasons why tastes are Beauchamp’s team recently discovered that Another example of tasteto loss closer lies 1 inaletter to 3 . What’s more, carried six species Nature.

2 . All cats. All ------

SOPHIE CASSON /THREE IN A BOX TASTE OUTLOOK

the ability to taste food, and ignores the role The super- branched off from decades later, researchers finally identified the of these receptors in other parts of the body tasters among other fish 400 million gene responsible for PTC sensitivity, called (see ‘Hardwired for taste’, page S7). There is the animal years ago. Sharks lack T2R38, and confirmed that different versions no evidence that losing taste genes confers any world are bitter taste receptors, of the gene largely explain why not everyone advantages to an animal, although Schwenk is goldfish. suggesting that these can taste the chemical (see ‘The finer points of happy to speculate. “Most carnivores are scav- genes evolved more taste’, page S2). engers as well as predators,” he says. “They eat recently. Recent studies have refined Fisher’s ideas a lot of rotting flesh, so it might be good to not Bitter is perhaps the taste that most intrigues about how the variations in PTC sensitiv- taste it so well.” evolutionary biologists. It is the ‘Darwin’s finch’ ity evolved. A team led by Stephen Wooding, Pandas, a largely vegetarian member of of taste, elaborated and customized to suit a an evolutionary biologist at the University of Carnivora, lack umami receptors. The pandas’ species’ ecological niche. Humans have 24 or Texas Southwestern Medical Center in Dallas, bamboo-only diet gives them little need to 25 (depending on the person) different bitter repeated Fisher’s experiments6 using apples detect proteins, says Jianzhi Zhang, an evolu- receptors, each recognizing unique combina- spiked with PTC, instead of water solutions tionary geneticist at the University of Michi- tions of chemicals. (perhaps to avoid being spat at). Chimps gan in Ann Arbor, who reported this lack of still differed in their ability to taste the bitter receptors in 2010. His team also discovered that chemical, but DNA sequencing revealed that vampire bats have no sweet receptor, and that that cannot taste PTC have an all bats, including insectivorous species, lack entirely different mutation in T2R38 from umami receptors4. Zhang’s team has also been human non-tasters — their insensitivity unable to find working sweet-receptor genes in evolved independently. several species of birds, grass-eating horses and One of the compounds that T2R38 rec- KEREN SU/ GETTY IMAGES KEREN SU/ GETTY omnivorous pigs — a pattern he finds puzzling. ognizes, , is abundant in , such as broccoli and Brussels DEVONIAN TASTES sprouts. Goitrin can worsen hypothyroidism, The sense of taste must have carried an evolu- a condition caused by low iodine intake. Vari- tionary advantage to have evolved in the first ation in sensitivity to PTC and goitrin might place. Beauchamp says that taste-sensing sys- persist because it could help iodine-starved tems in the mouth perform two essential tasks: populations avoid hypothyroidism and obtain umami and sweet detection help animals find nutrients from vegetables. energy-dense nutrients, and bitter detection Diet is not the only driver of change in bit- helps them avoid toxic substances. Scientists ter-tasting ability, however. Geneticist Sarah know far less about the biology and evolution of Tishkoff’s team at the University of Pennsylva- sour and salt tastes. One theory is that detecting nia in Philadelphia recently tested7 hundreds salts helps an animal control its levels of sodium of individuals from 57 human populations in and other ions, whereas sour tastes help it avoid Central and West Africa. They found both PTC the acids in unripe fruit and spoiled foods. tasters and non-tasters, but there was no obvi- All vertebrates have some ability to avoid ous correlation with their different diets. toxic chemicals and seek out nutrients. By com- In the past decade, scientists have discovered paring animals from different branches of the sweet receptors in the gut that influence insu- evolutionary tree, scientists have inferred that lin levels, and bitter receptors in the lungs that taste probably evolved more than 500 million A strict bamboo diet might have stripped the can clear inhaled substances. Tishkoff’s team years ago — before land vertebrates, bony fish, panda of the umami . suggests that roles such as these, and not diet, sharks and lampreys diverged — when their might explain the evolutionary differences in common ancestor, a primitive fish, developed Toxic bitter compounds come in all shapes PTC tasting. Zhang also thinks there is more a new kind of cell. and sizes, so it makes sense that the recep- to the evolution of taste than just flavour. He Taste buds have been repeatedly tweaked tors that recognize them are diverse, says suggests that researchers use model organ- over time to suit various animals’ dietary needs, Beauchamp. Bitterness is code for danger, isms, such as mice lacking various taste genes, says Thomas Finger, co-director of the Univer- but many bitter compounds also provide to understand the roles of these receptors. sity of Colorado’s Rocky Mountain Taste and important nutrients. For example, during the “We’re finding a lot of mismatches between Smell Center in Aurora. Many fish are covered lean winter months, the Japanese macaque feeding ecology and taste-receptor evolution,” with taste buds. “The super-tasters among the supplements its diet by eating willow trees. he says. “Perhaps we still do not have a com- animal world are goldfish,” says Finger. “Gold- The bark of the willow contains salicin, plete understanding of the functions of those fish and catfish have way more taste buds than which tastes bitter to many animals. A recent genes — or of taste.” ■ anybody else.” They have poor vision, and their study of the bitter receptor T2R16, which taste buds, including those on their whiskers, is common to all primates, reported that Ewen Callaway is a news reporter for Nature could help them sense their way to a meal in the macaque version is the least responsive in London. murky water, he adds. to salicin5. The evidence suggests that umami recep- Bitter taste evolution, then, is also about dis- 1. Fisher, R. A., Ford, E. B. & Huxley, J. Nature 144, 750 (1939). tors were the first to develop. In 2008, Zhang’s tinguishing between different chemicals. “If 2. Li, X. et al. PLoS Genet. 1, e3 (2005). team reported the discovery of genes, similar to you go out into the real vegetable world, what 3. Jiang, P. et al. Proc. Natl Acad. Sci. USA 109, 4956- those that encode recep- you’ll find is that almost everything is bitter,” 4961 (2012). NATURE.COM tors used by humans and says Beauchamp. “An animal that rejects every- 4. Zhao, H. et al. Genome Biol. Evol. 4, 73–79 (2011). Ever craved soil? mice to sense the amino thing that’s bitter would be in trouble.” 5. Imai, H. et al. Biol. Lett. doi: 10.1098/rsbl.2011.1251 (2012). Evolutionary theory acid glutamate, in the This principle could explain Fisher’s discov- 6. Wooding, S. et al. Nature 440, 930–934 (2006). might explain why: genome of the elephant ery that some individuals, among both humans 7. Campell, M. C. et al. Mol. Biol. Evol. Doi: 10.1093/ go.nature.com/1duag4 shark, a species that and chimps, are unable to taste PTC. Seven molbev/msr293 (2011).

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