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The Mysterious Origin of the Sweet

On its way to a grocery counter near you, this delicious traversed continents and mastered coevolution

Barrie E.

pples! You can find more than a and roses no fewer than fourteen.) vectors and that a female bee can forage Adozen varieties in the fruit section Does it have relations in the wild crab for up to three kilometers. of your local grocery, or spread out in of North America such as the Little wonder that there may be, a stall by a farm gate on a back road— garland ( coronaria) or in throughout the temperate world, per- maybe even in your own yard in au- in the wild crab (Malus sylves- haps 20,000 distinct named apple vari- tumn. You’ll likely know the names tris)? Does it owe its size to some gross eties. There are, by contrast, only two of your favorites: , McIntosh, chromosomal change like polyploidi- varieties of commercial and just Delicious. If you live in Western zation or a splitting or loss of existing one of the kiwifruit. Moreover, with al- Europe the selection might include chromosomes? Was it a chance discov- most no exceptions, every single apple , Cox’s Orange Pippin, ery, like the kiwifruit, from a source pip has the potential to grow into a new , Holstein or Ribston of nutritionally relatively indifferent apple tree—there are virtually no sterile Pippin. Abundant apples ready for the wild ? The answer in every case apples. Elite apples from this genetic ka- eating can likewise be found in Eastern above is no, but the truth is perhaps leidoscope may be grafted to preserve Europe and on through to the Chi- even stranger. their exact genetic character, but this is nese border and the Gobi desert. You Remarkably, the parentage of every not essential. Apple on their own can grow this delicious fruit, with its single one of the apple varieties list- roots are perfectly viable. On the other very high levels of and valu- ed above is unknown. hand, very many other commercial fruit able antioxidants, in your own back emerged by chance in an Iowa fence crops, such as navel oranges and com- lot in almost any soil; you can store it row. It was spotted in about 1870 and mercial , are totally sterile and in the cellar throughout the harshest bulked up by the Stark Nursery Com- rely, eternally, for their genetic future of winters, and it will retain its pany. Golden Delicious (no relation and spread, on or some other and value into the early spring. You except that it’s an apple) emerged as form of clonal propagation. may cook it, dry it or ferment it as you a chance seedling, in about 1890, in a choose, but it is one of the very few hedgerow in West Virginia. It gained a The Geological Framework sources that you can pick, ripe particular claim to fame by being cloned Long ago, probably some time between from the tree, and eat without any into millions of grafted young trees by the end of the Cretaceous and the early preparation, peeling, grinding, hulling the officers of the Marshall Plan, and Tertiary period (about 65 to 50 million or other manipulation. exported, after 1945, to revive the fruit years ago), the ancestors of the apple But what is this valuable and versa- industry of Western Europe. Figure 1. Apples are so ubiquitous that we tile fruit, and where did it come from? It seems that many of our favorite may be tempted to take them for granted. Yet Is it the product, like so many plants, apples have arisen by sheer chance. So their diversity and broad geographic distribu- of the hybridization of numerous par- what is the arithmetic basis of this lot- tion actually pose fascinating scientific ques- ents from distant lands? (Wheat has at tery? The secret to the apple’s origin tions. Why are there perhaps 20,000 varieties least three parents, two lies in the fact that apple trees cannot of apples but only two commercial varieties normally pollinate themselves. Unlike, of bananas and one of kiwifruit? Is the sweet Barrie E. Juniper is Emeritus Reader in say, peaches, which can and do self-pol- apple related to the so-called crabs? Were cur- sciences at the University of Oxford and Fellow linate, predictably producing peaches rently important commercial varieties—Red Emeritus of St. Catherine’s College, Oxford. His virtually identical to the parents, the vi- and Golden Delicious, for example—de- research has included explorations of plant sur- able (or pips) will produce apples, veloped by hybridization or chromosomal changes? For that matter, where in the world faces, including the specialized ones of insect-eating some of which may have value—but carnivorous plants, and the interactions between did the apple come from? The author’s probe people, their animals and the evolution of crop none of which will resemble the par- of these and other mysteries of the apple’s plants. He and his coauthor, David J. Mabberley, ents. Imagine the evolutionary power origins takes us to a remote mountain range recently published The Story of the Apple (Tim- of the multiplicity of potential crosses in and introduces us to power- ber Press, 2006). Address: University of Oxford, in planted or wild . Then mul- ful evolutionary drivers such as the bear and Oxford, OX2 6JF, U. K. Internet: barrie.juniper@ tiply this potential by the fact that a horse. (Photograph courtesy of Keith Weller/ plants.ox.ac.uk range of bee may act as USDA Agricultural Research Service.)

© 2007 Sigma Xi, The Scientific Research Society. Reproduction 44 American Scientist, Volume 95 with permission only. Contact [email protected]. © 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 January–February 45 with permission only. Contact [email protected].

KAZAKHSTAN MONGOLIA to emerge as a distinct geological fea- ture about 12 million years ago, and it is still lengthening and rising. In places, in TAKLAMAKAN those “heavenly mountains” (that is the DESERT translation), if you stand in one place, you may be 1.5 centimeters higher at FERGANA Xi’an the end of the year than you were at the VALLEY beginning. The Tian Shan has by now lifted its peaks well above the snow Shanghai line and lies as a great mountain range about 1,600 kilometers miles long and 640 kilometers in depth, running from what is now China in the east to Uz- bekistan in the west. The east-west ori- entation, with about 20 parallel ridges, is important to our story. The vast mass of the Indian Ocean to the south, through the constant Figure 2. Ancestors of the sweet apple probably crossed a land bridge between North America warm monsoons, has kept the region and Asia, settling into central China near what is now the city of Xi’an. A few million years ago, these neo-apples made their way westward into the Tian Shan range. Red lines are trade ice free. The warming influence of routes along which the apple later spread. these monsoons, in due season, can be detected deep into China. Unlike migrated west across the land bridge tral China, roughly in the area of the the continental regions of northern Eu- connecting what is now North America current provinces of Xi’an and , rope and North America, the whole of with Asia. Although the Bering Strait and perhaps in a great corridor of Ter- the Tian Shan and regions to the south is currently a shallow sea with many tiary temperate forest, a recognizable have not, at least in the immediate geo- islands, during at least 12 periods in ancestral apple. logical past, suffered glaciation. Large the immediate geological past, seawater Much earlier, about 40 million years continental areas, as anybody who has was locked in glaciers and ice sheets, ago, the Indian subcontinent, which spent a night in the desert will testify, and the two continents were connected had detached from East Africa, crashed lose heat very rapidly. Thus northern by an ice-free bridge. Plants and ani- into the great northern land mass. Just Europe and North America chilled out mals would have moved, in both di- like something pushing gently on the rapidly along the advance of the ice rections, through “Beringia” to their edge of a carpet, this thrust successively fronts, as, time after time, the glaciers present locations. This little neo-apple drove up the Himalayas, the Pamirs moved deep to the south. would probably have looked more like and the Tian Shan. India is still moving As a result of its “defense” by the a hawthorn () with bunches northward at several centimeters a year, warm Indian Ocean over millions of of long-stalked not much bigger as the mountain peoples of northwest years, the Tian Shan has become a than peas. But by about 10 million to India, Kashmir, and Ta- refuge for the sustained evolution of 12 million years ago there must have jikistan know full well. The Tian Shan, plants and animals. Almost no other existed somewhere in what is now cen- the last of the ripples as it were, began area in the world has remained invio- late for so long. In contrast, most of North America and the British Isles and much of Western Europe were scraped clean by ice little more than 10,000 years ago. The spiky, perma- nently snow-covered peaks of the Tian Shan bear testimony to their ever-rising altitude and lack of glacial scraping. The mountains are constantly expos- ing new geological facies, disturbing existing drainage systems, wrecking existing patterns of vegetation and yet at the same time exposing fresh soil sites for exploitation by incoming seedlings. There is no geological peace in this fault-riven zone, from the In- dian border to the edges of the great steppe lands of . Into this geologically restless but fe- Staton R. Winter/Getty Images Winter/Getty R. Staton cund environment moved, principally Figure 3. The Tian Shan is the most recent mountain range to emerge from the collision of India from the east, the ancestors of thou- with Asia. Currently rising at about 1.5 centimeters per year, the Tian Shan has never experienced sands of present-day plants, including glaciation. Snow-covered peaks provide abundant moisture to fruit forests in the valleys. those of many important crops and,

© 2007 Sigma Xi, The Scientific Research Society. Reproduction 46 American Scientist, Volume 95 with permission only. Contact [email protected]. alongside them, many animals includ- cene Epoch of the Tertiary, at least 5.3 ing bear, deer and wild pig. In the for- million years ago. est with these neo-apples would have Given this geological turmoil, it developed apricots (Prunus armenai- should be no that the indi- ca), (Pyrus spp.), pomegranates vidual species of the fruit forest are not (Punica granatum), figs (Ficus), cher- long-lived trees; 30 years produces a ries (Prunus avium and cerasus) and the fully productive apple specimen, and mulberries (Morus). To the west and 100 years is about the maximum age south this new, mixed “fruit forest” that an apple, or apricot tree could would have been augmented by the normally be expected to survive. There walnut ( regia). is no premium on evolving, say, the Among the vegetation colonizing longevity of a bristle-cone pine when the Tian Shan came, likely via birds your habitat is likely to disappear un- from the east, the ancestors of what we der an enormous rockfall or outwash know as the “sweet” apple. The fruit fan well within a hundred years. probably then looked like a tiny, long- stalked, bitter apple something like The Evolutionary Scene , the Siberian crab. The From a neo-apple the size of a small pips may have been carried in a bird’s grape, as we suppose the first coloniz- crop or clotted onto feet or feathers. ers to be, we now have, on our mar- A carrier-bird candidate is the beauti- ket shelves or in our gardens, a sweet ful azure-winged magpie (Cyanopica apple the size of a tennis ball or even Figure 4. On arrival in the Tian Shan, the neo- cyanus), which now occurs as relict but a softball. apple likely resembled the tiny, long-stalked, virtually identical populations at both Left behind, in both the evolution- bitter apple Malus baccata, the Siberian crab. ends of the transcontinental forest in ary and geographical sense, is the (Illustration courtesy of Rosemary Wise.) southern Europe and eastern China. spectrum of other apple species, some- It is, of course, impossible precisely times crudely known as “crabs” and America and a few in Europe. These to date this invasion, but we can be perhaps as many as 30 distinct species. crabs (Saxon for bitter or sour), as they sure that the players, both plant These wild species are found princi- are sometimes derogatorily defined, and animal, had found a place in the pally in Central China (see Figure 8), are often of considerable decorative rising Tian Shan some time in the Mio- but with substantial numbers in North value—some have indeed played a

uplift apple erosion pips

Figure 5. Forces driving the evolution of the sweet apple include the rapid uplift and erosion of the Tian Shan, producing fertile soils watered by melting snows (upper left). Into this rich environment, transported most likely by birds, came apple pips from central China (upper right). Indeed, the forests that developed in the valleys of the Tian Shan are rightly called fruit forests because of their abundant fruit-tree species. Along with the fruit came bears, who found the caves in the mountainsides and the forests below a wel- coming habitat (left). Because smaller apples pass through bears (and to a lesser extent, wild horses) without dissolving the placenta, the pips of smaller apples were unable to fertilize, selecting for larger varieties.

© 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 January–February 47 with permission only. Contact [email protected]. migrated into the Tian Shan. As the endocarp mountain ranges began to rise, the na- ture of the geology would have pro- vided an Elysium for bears and other forest-dwelling animals. To the east, be- pips yond the Gobi desert where practically nothing can live, the flat loess-coated lands of China may be suitable for ag- riculture but provided no suitable habi- tat for cave dwellers. The unglaciated slopes below the Tian Shan ice pack are a perfect habitat, particularly where mesocarp caves are washed out of the softer rocks by the constant flow of meltwater. A slice through a section of the Tian Shan exocarp would reveal cavities like the inside of a Gruyère or Emmenthaler cheese. Figure 6. Apple anatomy, shown in longitudinal and latitudinal cross sections, features a Tian Shan bears have an impressively central placenta that contains the pips, along with inhibitory agents that prevent the pips catholic diet—from wild rhubarb in the from germinating in situ. Only when the placenta is broken and the pips dispersed do apple spring, through bee grubs and honey seedlings emerge. in the late summer to apples in the fall. Those long, rake-like claws not only part in ornamental plant breeding— is, as we have seen, not a problem. The serve to catch fish, dig for roots or tear but the fruits are sour, sometimes even turnover of individual trees is likewise open bee nests, which are abundant in intolerably bitter and astringent. Thus conducive to the rapid evolution of a the Tian Shan, but they also serve as they are of scant culinary value and, tree species, as is the fact that sweet garden rakes to harvest large or small as we shall see later, seem to have con- apples are now, at least for all practi- fruit in quantity. North American black tributed little if anything to the gene cal purposes, self-incompatible—that and brown bears (Ursus americanus and pool of the sweet apple. is, they cannot pollinate themselves. Ursus arctos) consume large quantities What natural features of the unique Therefore each apple tree within the of fruits of all kinds in the fall, selecting Tian Shan might have contributed to forest and even each pip, usually five, the larger fruits or larger clusters. If we this rigorous selection program? Time within each individual fruit will be re-interpret this selection pressure to different. There are many apples on a another continent, noting that this ac- mature tree, so natural selection has tivity not only enhances the bear’s food a rich and diverse population upon intake but also unconsciously selects for which to work. larger and larger fruits or bunches, we Birds, of course, eat all manner of can comprehend the observed increase fruit. But most birds eat seeds—a di- in the size of the apple. etary feature not conducive either to Over millions of years, millions of the selection or spread of a . bears just prior to hibernation slowly Sweet apples are often eviscerated and unconsciously selected the larger by birds, but the seeds are frequently and sweeter fruits of the neo-apples. left in the empty shell of the pome. Bears do have a sweet tooth, as A. A. The reason is that apple (and pear Milne noted in Winnie the Pooh. The and ) seeds are rich in cyano- relative inefficiency of a bear’s jaw , which are highly repellent, in crushing fruit has another unin- particularly to birds. If you wish, you tended consequence. As we have seen can smell a whiff of as you above, seeds that remain within the crunch two or three seeds between tissue (placenta) of the apple do not your teeth, but you would need a cup- germinate. Herb Aldwinckle of Cor- ful of seeds to do yourself any harm! nell University told me he has noticed Moreover the placenta of the apple that very small apples pass intact and fruit, the womb, contains inhibitory uncrushed through a bear’s jaws and substances that prevent the germina- gut and, in one or two cases, were seen tion of the apple in situ. This is a intact in the fecal mass. The seeds in

Regis Cavignaux/ BIOS / Peter Arnold, Inc. Arnold, Peter / BIOS Cavignaux/ Regis commonly observed phenomenon in the small intact fruits would not have fruits as Michael Evenari showed in germinated. It does not pay, in a ge- Figure 7. Ursus arctos arctos, the Eurasian or European brown bear, was likely the driv- 1949. So what then does, or did, dis- netic sense, to be a very small apple ing force behind the development of Malus tribute the original apple seed? in the Tian Shan. Compared to their pumila, the sweet apple. Its long claws are counterparts of the North American well adapted to gathering fallen fruit, and The Engines of Evolution continent, the bears (and the apple the catholic diet of all brown bears is well The bear. Through the Miocene it would trees) and other inhabitants of the Tian established. seem that brown bears (Ursus arctos) Shan would have had 1,000 times as

© 2007 Sigma Xi, The Scientific Research Society. Reproduction 48 American Scientist, Volume 95 with permission only. Contact [email protected]. long to indulge in some sort of mutual TIAN SHAN selection pressure. Wherever they are, 37 bears learn quickly. The brown bears of Montana are known, as the artist Ja- 11 net McGahan saw in 2001, to seek out and feed on the sweeter fruits of the grafted apple trees (imported Malus pumila) in planted orchards. The jaws and guts of a bear, as 12 Traveset at the Mediterranean Insti- /TIBET 10–13 XI’AN tute for Advanced Studies and her co- 10–13 workers have shown, do little or no SICHUAN damage to the teardrop-shaped, hard 19 and tannin-coated apple pip. Traveset’s group examined a wide range of gut- transmitted seeds, and in virtually ev- YUNNAN 20 ery case the viability of the seeds was 16 either neutral or enhanced. The fecal loads are dumped all over the Tian Shan in the fall—in a fertile mix of nitrogen- rich compost and, we have demonstrat- ed in trial plots, carrying bear-viable apple seed. Then we suppose that, as on every other continent in the world, a spectrum of hard-working dung beetles Gobi desert broad-leaved forest of the warm temperate zone will disperse, in their various ways, the alpine vegetation of the steppe whole fecal mass along with its fellow- Quinghai-Tibetan Plateau traveling seeds. mixed and coniferous and deciduous tropical monsoon rain forest Thus, probably over the whole of broad-leaved forest of the temperate zone the Tian Shan but particularly on the subtropical broad-leaved northern slopes where the summer’s forest heat was less fierce, there emerged, over Figure 8. Areas of what was once forested central China are rich in Malus, with perhaps 37 dis- millennia, an extraordinarily large ap- tinct species. The numbers under the titles of provinces give an indication of this richness. On the ple, often sweet-textured and invariably other hand, the Tian Shan has only one dominant species, namely or M. Pumila, with a very short stalk. The German/ but the varietal richness of this species is almost infinite, far exceeding that of any other apple. Russian explorer Johann or Ivan Sievers in 1793 discovered this apple. But he the horse probably would have ranged key were domesticated, as elucidated by died shortly after discovering both the farther and more widely than the bear Carles Vila and his colleagues at Uppsala apple and the fruit forests. It was not before dropping its fecal load. University, in what is now Kazakhstan until 1830 that Carl Friedrich von Lede- But it is unlikely that the horse was some 7,000 years ago. In the guts of both bour in his new Flora Altaica named this a major engine for apple selection. horse and , directed by human apple in honor of his late colleague Siev- Horses will not willingly penetrate travelers, the apple pip moved west. The ers—Malus sieversii. This name is widely into thick forest, and knowledge of the sharp hooves of these animals unwit- found in the literature. But it has more resident bears would have kept them tingly planted the apple pips at every recently been discovered that the same wary. They may have browsed on the oasis. The east-west ridges of the Tian apple, one of many that had escaped to fruit but would have moved away to Shan, with rich valleys and their for- the West over the previous thousands of the safety of the open plains at night tuitous patches of fruit forest between, years, had been named by Philip Miller and commonly shed the seed upon would have determined the direction of in the United Kingdom in 1768 as Malus stony ground. Nevertheless, long be- the emerging trade routes. It is likely that pumila, and, by reason of priority, the fore their by early humans these trade routes—later to be known as name M. pumila must take precedence. they may also have moved to the graz- the “Silk Roads,” but actually in use long The wild horse. Wild horses, which ing land around ancient oases, where before silk was invented—began as ani- likewise had migrated from North their sharp hooves might have thrust mal-migration tracks leading from one America over Beringia, would have seeds into the ground to establish new oasis or rich grazing ground to another. developed a taste for the wild apples wild orchards. Wild horses may thus on the margins of the new fruit forests. have contributed in a small way to the The Evidence from the DNA Sándor Bökönyi of the Archaeological spread and diversification of the fruit But if the earliest travelers, with their Institute of the Hungarian Academy components of the fruit forests and the newly domesticated horses or don- of Sciences believes that a few truly mixing of the apple gene pool at least keys, began to travel westward from wild horses may still survive in the on the edges of the forest patches. one oasis to another, is it not likely that vast plains of Kazakhstan. The horse’s The domesticated horse. Once equines the emerging sweet apple of the Tian jaw and gut, like that of the bear, do were in human employ, the whole sce- Shan could have hybridized with other no harm to an apple pip. Moreover nario changed. The horse and the don- species of apples that lay in its path as

© 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 January–February 49 with permission only. Contact [email protected]. chloroplast it traveled west? Sporadically within nucleus the Tian Shan can be found Malus bac- cata. In Khirgistan can be found Malus khirgizorum. As the apple, this welcome economic migrant, reached eastern Eu- rope, it would have come within the range of M. trilobata in the Levant, with M. florentina in and with M. syl- vestris over most of the more northern lands of western Europe. Yet it does not seem, as Els Coart with the Ag- ricultural Research Centre in Ghent and her colleagues discovered, that ei- mitochondrion ribosomal DNA ther by accident or by intent was there repeats any significant gene flow between M. pumila and any other apple species. The timing of the flowering period of rbcL M. pumila is not dissimilar to any other apple species. The only feature unique 18S 5.8S 28S IGS to M. pumila among all species of Ma- matK lus seems to be that it lacks, or virtually 1R 1R ITS-1ITS-2 lacks, an endosperm. This might, as Liliana Costa and her colleagues here chloroplast DNA at Oxford have suggested, through Figure 9. Two types of DNA prove useful in developing phylogenies of apple varieties. Chlo- epigenetic control, determine a choice roplast DNA can readily be extracted from chloroplasts, whereas nuclear DNA, including the of partners. ribosomal internal transcribed spacer gene (ITS), can be garnered from the cell nucleus. In plants, there are three sources of DNA within every cell, all of which can be used to detect relationships 18-base-pair through their . In this study duplication series Malus section Malus both the nuclear and the chloroplast series Baccata ] wild apple section Sorbomalus domesticated apple DNA have proved useful (see Figure section Briolobus 9). The chloroplast DNA provides data section Docyniopsis Malus micromalus about the evolutionary relationships of section Chloromeles the maternal line because chloroplasts Malus baccata weak (50–74 percent) support in Malus and in most higher plants strong (75–100 percent) support duplication polymorphic are transmitted to the next generation duplication absent through the eggs. Any evidence of hy- bridity may be revealed by the nuclear Malus prattii DNA, and, fortunately, the DNA from Malus is readily extracted. Malus kansuensis As Stephen A. Harris, Julian P. Robinson and I have shown, both the Malus delavayi wild apple, represented through di- rect collections of material in the Tian Shan, and domesticated apples cluster closely together, as a phylogeny based Malus florentina on the ribosomal internal transcribed maloid outgroups spacer (ITS) gene shows (Figure 11). Duplications in the matK gene (Figure matK 3' trnK 10) indicate that from very different lo- cations in the Tian Shan, there were at least two separate importations of wild apples from the region—in all prob- aaattctatttaaatattaaataattaagagataacaaaaaattaagagataacaaaaaattaat ability there were many more. The oc- 18-base-pair duplication currence of these two shared 18-base- pair duplications and the absence of Figure 10. Phylogeny of the chloroplast-encoded gene matK shows two 18-base-pair duplica- these duplications in M. sylvestris, of- tions present only in Tian Shan wild apples and domesticated apples, pointing to the Tian Shan ten cited as a potential partner, as the original source of Malus pumila. Apple is quite complicated, owing in part to show the close affinity of the wild Tian the thousands of varieties. Two to taxonomic hierarchy—section and series between Shan apple with the sweet apple. Note and species—help distinguish these plants. In this and Figure 11 the circles refer to the too that the other European species M. degree of statistical support for groupings. (Adaped from Harris, Robinson and Juniper 2002.) trilobata and M. florentina lie far away

© 2007 Sigma Xi, The Scientific Research Society. Reproduction 50 American Scientist, Volume 95 with permission only. Contact [email protected]. from any possible recent phylogenetic domesticated apple series Malus section Malus relationship. In the ITS diagram, M. series Baccata ] domesticated apple niedzwtzkyana is considered now to be section Sorbomalus wild apple just a rare colored form of the wild section Briolobus Malus orientalis apple and M. orientalis and M. pruni- section Docyniopsis wild apple Malus asiatica folia are no more than local variants of section Chloromeles weak (50–74 percent) support domesticated apple the wild apple. strong (75–100 percent) support domesticated apple wild apple Migration to the West wild apple As horse transport developed along wild apple the east-west trade routes, this “new” Malus niedzwetzkyana apple, a welcome migrant, would have Malus orientalis moved into areas that were already at a fairly high level of sophistication in domesticated apple Malus niedzwetzkyana agricultural terms. The Fergana Val- Malus baccata ley, now in Uzbekistan, was one of the first areas in the world where the Malus sieboldii pioneer techniques of , the Neolithic revolution, were practiced. Malus hupehensis The tracks would have led onward to Malus toringoides higher, cooler lands—not, at first, into the steaming hot Tigris-Euphrates val- Malus yunnanensis ley—on the northern edges of the great Malus prattii Malus yunnanensis Persian empires. The new apple would Malus honanesis have found both fertile ground and, Malus kansuensis in all likelihood, ready acceptance as Malus fusca a new fruit to add to the already well- Malus ombrophila established fig, date and vine. Malus florentina Malus trilobata It seems possible that grafting was Malus tschonoskii invented in the Tigris-Euphrates valley, perhaps around Babylon, as irrigation Malus coronaria and tropical heat raised the salinity Malus ioensis of the soil. A combination of salt-tol- Malus doumeri maloid outgroups erant stocks with indifferent grapes, was found to be able to support, on Figure 11. Phylogeny of the nuclear ribosome internal transcribed spacer (ITS) gene helps a graft, high-quality grapes with low group various apple varieties. Further, these groupings show that wild apples (Malus sieversii) salt tolerance. The technique would from central Asia are quite similar to domesticated apples, and that several other Malus spe- readily have been transferred to other cies are nearly indistinguishable. (Adaped from Harris, Robinson and Juniper, 2002.) top fruit, including apples, which were growing in the cooler, higher ground phism and microsatellite markers. Molecular Traveset, A. 1998. Effect of seed passage to the north. Both seedling and grafted Ecology 12:845–857. through vertebrate frugivore’s guts on Costa, L. M., J. F. Gutierrez-Marcos and H. germination: A review. Perspectives in Plant apples began to move into Europe. Ecology, Evolution and Systematics 1:151–190. From Europe the apple moved across G. Dickinson. 2004. More than a yolk: The short life and complex times of the plant en- Vila, C., J.A.Leonard, A. Gotherström, S. the seven seas. And now, through its dosperm. Trends in Plant Science 9:507–514. Marklund, K. Sandberg, K. Lidén, R.K. immense fecundity and diversity, the Dewey, J. F., M. Shackleton, C. Chengfa and Wayne and H. Ellegren. 2001. Widespread sweet apple, Malus pumila, is not only S. Yiyin. 1988. The tectonic evolution of origin of domestic horse lineages. Science one of the major crops of the temperate the Tibetan Plateau. Philosophical Transac- 291:474-477. zone, but seedling apples, sometimes tions of the Royal Society of London, Series A Welch, C. A., J. Keay, K. C. Kendall and C. T. of high quality, continue to emerge 327:379–413. Robbins. 1997. Constraints on frugivory in in hedgerow, ancient trackway or Evenari, M. 1949. Germination inhibitors. Bo- bears. Journal of Ecology 78:1105–1119. neglected gardens, defying both the tanical Reviews 15:153–194. grasp of agribusiness and the imposi- Hanski, I., and Y. Cambefort, eds. 1991. Dung tion of government diktat. Beetle Ecology. Princeton University Press. Harris, S. A., J. P. Robinson and B. E. Juni- per. 2002. Genetic clues to the origin of the Bibliography apple. Trends in Genetics 18:426–430. For relevant Web links, consult this issue Bökönyi, S. 1974. The Przevalsky Horse, trans- Juniper, B. E., and D. J. Mabberly. 2006. The Story of American Scientist Online: lated from the Hungarian by Lili Halápy. of the Apple. Portland, Ore.: Timber Press. London: Souvenir Press. http://www.americanscientist.org/ Coart, E., X. Vekemans, M. J. M. Smulders, I. McGahan, J. 2001. Another apple for Snow IssueTOC/issue/921 Wagner, J. van Huylenbroeck, E. van Bocks- White. Pomona 34:10–11. taele and I. Roldán-Ruiz. 2003. Genetic vari- Traveset, A., and M. F. Wilson. 1997. Effect ation in the endangered wild apple (Malus of birds and bears on seed germination of sylvestris (L.) Mill.) in Belgium as revealed fleshy-fruited plants in temperate rainfor- by amplified fragment length polymor- ests of southeast Alaska. Oikos 80:89–95.

© 2007 Sigma Xi, The Scientific Research Society. Reproduction www.americanscientist.org 2007 January–February 51 with permission only. Contact [email protected].