The Dispersal of Ancient and Modern Apples by Humans and Other Megafauna

Crop domestication often involves selection for larger fruits. In some crops, humans took plant species with relatively small fruits and, over many generations of artificial selection, developed a plant with much larger fruits. Consider giant pumpkins as an extreme example. Yet in the case of apples, relatively large fruits already existed in the wild. Producing larger apples happened quickly and, perhaps even, unconsciously. Apples were practically primed for domestication, and as Robert Spengler explains in a paper published last year in Frontiers in Plant Science, looking back in time at the origins of the apple genus, Malus, can help us understand how the apple we know and love today came to be.

Apples are members of the rose family (Rosaceae), a plant family that today consists of nearly 5000 species. According to the fossil record, plants in the rose family were found in large numbers across North America as early as the Eocene (56 – 33.9 million years ago). They were present in Eurasia at this time as well, but Spengler notes, “there is a much clearer fossil record for Rosaceae fruits and seeds in Europe and Asia during the Miocene and Pliocene (20 – 2.6 million years ago).” Around 14 million years ago, larger fruits and tree-form growth habits evolved in Rosaceae subfamilies, giving rise to the genera Malus and Pyrus (apples and pears). Small, Rosaceae fruits were typically dispersed by birds, but as Sprengler writes, “it seems likely that the large fruits [in Malus and Pyrus] were a response to faunal dispersers of the late Miocene through the Pliocene of Eurasia.” Larger animals were being recruited for seed dispersal in a changing landscape.

Glacial advances and retreats during the Pleistocene (2.6 million – 11,700 years ago) brought even more changes. Plants with effective, long distance seed dispersal were favored because they were able to move into glacial refugium during glacial advances. Even today, these glacial refugium are considered genetic hot spots for Malus, and could be useful for future apple breeding. As the Pleistocene came to a close, many megafauna were going extinct. This continued into the Holocene. Large-fruited apple species lost their primary seed dispersers, and their ranges became even more contracted.

Humans have had an extensive relationship with apples, which began long before domestication. Foraging for apples was common, and seeds were certainly spread that way (perhaps even intentionally). Favorable growing conditions were also created when forests were cleared and old fields were left fallow. Apple trees are early successional species that easily colonize open landscapes, gaps in forests, and forest edges, so human activity that would have created such conditions “could have greatly promoted the spread and success of wild Malus spp. trees during the Holocene.”

The earliest evidence we have of apple domestication (in which “people were intentionally breeding and directing reproduction”) occurred around 3000 years ago in the Tian Shan Mountains of Kazakhstan, where Malus sieversii – a species that is now facing extinction – was being cultivated. This species was later brought into contact with other apple species, a few of which were also being cultivated, including M. orientalis, M. sylvestris, and M. baccata. These species easily hybridized, giving us the modern, domesticated apple, M. domestica. As Spengler writes, “the driving force of apple domestication appears to have been the trans-Eurasian crop exchange, or the movement of plants along the Silk Road.” Continued cultivation and further hybridization among M. domestica cultivars over the past 2000 years has resulted in thousands of different apple varieties.

The unique thing about domesticated apples is that their traits are not fixed in the same way that traits of other domesticated crops are. Growing an apple from seed will result in a very different apple than the apple from which the seed came. Apple traits instead have to be maintained through cloning, which is accomplished mainly through cuttings and grafting. Apples hybridize with other apple species so readily that most apple trees found in the wild are hybrids between wild and cultivated populations.

Spengler considers the study of apple domestication to be “an important critique of plant domestication studies broadly, illustrating that there is not a one-size fits-all model for plant domestication.” The “key” for understanding apple domestication “rests in figuring out the evolutionary driver for large fruits in the wild – seed dispersal through megafaunal mammals – and the process of evolution for these large fruits – hybridization.” He notes that “domestication studies often ignore evolutionary processes leading up to human cultivation,” which, in the case of apples, involves “hybridization events in the wild” that led to the evolution of large fruits “selected for through the success in recruiting large megafaunal mammals as seed disperses.” Many of those mammals went extinct, but humans eventually assumed the role, selecting and propagating “large-fruiting hybrids through cloning and grafting – creating our modern apple.”

Excerpt from Fruit from the Sands by Robert N. Spengler:

Indeed, the relationship between apples and people is close and complex, spanning at least five millennia. The story of the apple begins along the Silk Road… In recent years genetic studies have resolved much of the debate over these origins. Nevertheless, the ancestry of the apple is highly complex. Cloning, inbreeding, and reproduction between species have created a genealogy that looks more like a spider’s web than a family tree. To growers, the beauty of the apple lies not in its rosy skin but in its genetic variability and plasticity, its ability to cross with other species of Malus and other distant lines of M. domestica, and the ease with which it can be grafted onto different rootstocks and cloned.

See Also: Science Daily – Exploring the Origins of the Apple


Interested in learning more about how plants get around. Check out the first issue of our new zine Dispersal Stories.

Improving Perennial Crops with Genomics

This is the twelfth in a series of posts reviewing the 17 articles found in the October 2014 Special Issue of American Journal of Botany, Speaking of Food: Connecting Basic and Applied Science.

Genomics: A Potential Panacea for the Perennial Problem by Kendra A. McClure, Jason Sawler, Kyle M. Gardner, Daniel Money, and Sean Myles

Compared to annuals, a small but significant portion of our food comes from perennial crop plants. “Approximately one eighth of the world’s total food-producing surface area is dedicated to perennials,” and while that may seem relatively small, there is a good chance that some of your favorite things to eat or drink are perennial crops (apples, bananas, coffee, citrus, sugar cane, coconut, avocados, olives, grapes, cherries, almonds…just to name a few). However, making improvements to and introducing new cultivars of perennial crops is considerably more challenging compared to annual crops simply due to the nature of perennials. This puts perennial crops at greater risk to threats like pests and diseases, climate change, soil degradation, and water and land shortages. Advances in genomics, “the collection and use of DNA sequence information,” could change this.

Because breeding efforts to improve perennial crops is so challenging, “only a small number of elite varieties become popular, and the amount of genetic diversity represented by commercially successful cultivars is therefore often low.” This suggests that there is incredible potential for improvement in these crops, as long as major hurdles can be overcome. Following is a list of some of those hurdles:

  • Time – Most perennial crops have “extended juvenile phases,” meaning they won’t produce fruit for as much as ten years, considerably delaying evaluation of the final product.
  • Space – Perennial crops, especially trees, are large compared to annual crops, so the area required for evaluation is extensive.
  • Infrastructure – “Many perennials require trellis systems, extensive land preparation, and substantial costs for specialized equipment and skilled horticultural labor.”
  • Complex Evaluations – Automated assessments are “either unavailable or poorly developed,” so evaluations that include “size, shape, color, firmness, texture, aroma, sugars, tannins, and acidity” require “tasting panels” to ensure that the final product “satisfies consumer demands.” This process is expensive, and it differs depending on whether the crop will be consumed fresh or processed.
  • Vegetative Propagation – “Many perennials suffer from severe inbreeding depression when selfed,” so cultivars are maintained through vegetative propagation. This is a plus, because it means that the fruits of perennial crops are reliably uniform, so growers and consumers know what to expect year after year. However, this also means that while pests and pathogens evolve, the crops do not, making them more susceptible to such threats. Additionally, the “long histories” of certain cultivars “discourages [growers] from undergoing the risk of trying recently developed cultivars.”
  • Consumer Preferences – “Consumers often exhibit an irrational reverence for ancient or heirloom varieties,” despite the fact that the development of new varieties can result in crops that are higher yielding, resistant to pests and diseases, tastier, more nutritious, more suitable for storage, and require fewer chemical inputs. This obsession with traditional varieties leaves a “tremendous amount of untapped genetic potential for the improvement of perennial crops.”
"Modern avocado breeding still depends heavily on open-pollination because of the difficulty associated with making controlled crosses." (photo credit: wikimedia commons)

“Modern avocado breeding still depends heavily on open-pollination because of the difficulty associated with making controlled crosses.” (photo credit: wikimedia commons)

Apart from issues of social and cultural preference, the challenge of breeding perennial crops comes down to time and money. Advances in genomics can help offset both of these things. Using DNA-based predictions, a plant’s phenotype can be determined at the seed or seedling stage. Genomics techniques can also be “used to reduce the generation time thereby enabling combinations of desirable traits to be combined on a timescale that is more similar to annual crops.” Below are summaries of specific areas discussed in the paper for using genomics in perennial crop breeding programs:

  • Reduction of Generation Time – This can be done using transgenic technology in ways that do not result in transgenic (GMO) cultivars. One method uses virus-induced gene silencing, in which a host plant is infected with “a virus that is genetically modified to carry a host gene;” the host plant then “attacks itself and uses its own endogenous system to silence the expression of one of its own genes.” Early flowering in apples has been induced after seedlings were inoculated with apple latent spherical virus that expresses a flowering gene derived from Arabidopsis thaliana.
  • Genetic Modification – Advances in genomics have brought us transgenic technology, and several commercial crops have been genetically modified using this technology. Most of them are annuals, but one perennial in particular, SunUp papaya, has been a major success. Its resistance to ringspot virus rescued the papaya industry from a devastating pathogen that “almost completely destroyed the industry in Hawaii.” Consumer disapproval, however, poses a major obstacle to commercial production of genetically modified organisms, and unless this changes, “their widespread use is unlikely.”
  • Marker-Assisted Selection – This is the “primary use of genomics in breeding.” The time between initial plant crosses and the introduction of a new cultivar can be dramatically shortened when genetic markers are used to determine the phenotypes of adult plants at the seedling stage. This technology is also useful when crossing domesticated plants with wild relatives, since genetic markers can be used to determine when desired traits are present in the offspring.
  • Ancestry Selection – After crosses with wild relatives, offspring may “perform poorly because wild germplasm often harbors numerous traits that negatively affect performance.” To overcome this, the offspring is crossed with cultivated plants until undesirable traits are eliminated. This is called backcrossing. Using marker-assisted selection, breeders can “select a small number of offspring in each generation that carry both the desired trait from the wild and the most cultivated ancestry.”
  • Genomic Selection – The success of marker-assisted selection is greatest when used for traits that are controlled by one or a few genes. However, many traits involve a complex set of genes. Genomic selection is a new technique that “uses dense, genome-wide marker data to predict phenotypes and screen offspring.” It is “especially useful for predicting complex traits controlled by many small-effect genes.” Genomic selection is in its infancy, so there are kinks to work out, but it is a promising technology for perennial crop breeding efforts.

The use of genomics will not replace every aspect of traditional perennial crop breeding and “should be viewed as a potential supplement…rather than a substitute.” Geneticists and plant breeders are encouraged to work together to develop and implement these technologies in a concerted effort to improve the crop plants that help feed the world.

"Despite the remarkable phenotypic and genotypic diversity in bananas," the Cavendish banana is responsible for the "vast majority" of banana production. (photo credit: wikimedia commons)

“Despite the remarkable phenotypic and genotypic diversity in bananas,” the Cavendish banana is responsible for the “vast majority” of banana production. (photo credit: wikimedia commons)