The Fruit Explorer Considers the Evolution and History of Citrus Fruits

To All,

The Place of Citrus Fruits Among the Plants

Citrus fruits are all of the fruits in the genus Citrus, which is in the family Rutaceae, the rue family. There are no citrus fruits that grow in the wild in New England, but we do have one member of the Rutaceae, the hop tree. A friend once told me that he had found a poison ivy tree. Poison ivy is extremely variable, but it was alarming to find that it was so protean that it could shape-shift into a tree. I went to look at the alleged poison ivy tree and found that it was a hop tree, which resembles poison ivy somewhat due to its three-leaf pattern. The phrase, "Leaflets three, let it be," is a pretty good guide, and you should adhere to it strictly unless accompanied by an expert, but this guideline is not fool-proof. Common plants with leaflets three that are not poison ivy include blackberry (thorns are the giveaway that this is not poison ivy), trillium, jack-in-the-pulpit, box elder, and hop tree. The first two pictures below illustrate the hop tree and the third poison ivy.

   

   

Standard Evolutionary Thinking

Now let's review the standard evolutionary story about how the members of a genus evolve. We start with what is called the basal member of the genus. This is the first member of the genus, and all of the members of the genus are descended from this basal member. Evolution takes place as mutations offer up new genes and natural selection reduces the incidence of some genes and increases others. Moreover, a species might get split in two by the rise of a mountain range, a change in course of a river, transport on a floating log, or any number of other mechanisms. Once split, each portion of this species can then evolve in different directions, and eventually they evolve enough so that they are two different species, and they would not intermix even if they came back into contact. As time passes, species rise and fall, and the basal member of a genus gives rise to a number of ancestors.

This standard evolutionary story is illustrated in the following diagram, which I have scanned from Michael J. Benton, Vertebrate Paleontology, second edition, 1997, p. 280. The basal member of the pictured group of birds, which contains most modern birds, is at point A at the far left. In this diagram time passes as you go from left to right, and you can see how lineages evolve. Any species only has one immediate ancestor, not two or more. Moreover, a key point is that lineages split but they do not come back together; there are no loops in this diagram. Since lineages do not come back together, they are kept separate, and this plays an important role in allowing the living world to be divided into species. (A problem with this particular diagram is that it does not show lineages dying out. I won't worry about this problem since extinctions are not important to this e-mail.) You can flip through books on evolution or paleontology and find hundreds of diagrams like this and not find a single diagram with a loop.

The Problem of Hybridization

The sad fact is that this standard story does not apply very well to plants. This story has been largely constructed by biologists that specialize in animals, and they give short shrift to plants. This animal chauvinism is a constant irritation to us plantologists. One way that this story breaks down  for plants is hybridization. The standard evolutionary story dismisses hybridization since it is claimed that various isolating mechanisms, as they are called, make hybridization between species uncommon. Consider three isolating mechanisms.

First, many different species are physically unable to mate. Insects are famous for this isolating mechanism since the sexual parts of the male and female form a lock and key mechanism, and each species is constructed so that the male genitalia (the key) is mechanically able to fit only the female genitalia (the lock) of the same species. (For this e-mail I decided to look into this more, so I read Menno Schilthuizen, Nature's Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us About Evolution, Biodiversity, and Ourselves, 2014. From pp. 36-41, I was surprised to find that the lock and key hypothesis, which had been received wisdom in biology for more than a century, had come under attack and that mainstream biologists now reject it. However, a generalized lock and key hypothesis, p. 188, still seems to be good; this is all I need for this e-mail, so I will not go into this further since I am not the insect genitalia explorer.)

Second, it might be that organisms could mate, but behavioral or other mechanisms keep them from doing so in the wild. Consider the example of hybrids of lions and tiger, called ligers and tigons, where a lion is the father of the former and a tiger of the latter. These hybrids can be produced in the artificial environment of the zoo, but no liger or tigon has ever been reliably observed in the wild since in a natural setting lions and tigers do not mate. (If you want to see a liger, go observe Hercules, who is immortalized in the Guinness Book of records as the heaviest cat ever recorded and who appears each year at King Richard's Faire in Carver, MA. Mei-Mei's niece Ellen was employed as a wench by King Richard's Faire in the 1980s.) The first picture below appears to be an authentic liger

   

   

   

Third, cross-species matings might occur and produce offspring, but the offspring might not be able to propagate, with the mule being a well-known example. In short, standard evolutionary thinking, dominated by animal chauvinists, dismisses hybrids as of little importance. 

When it comes to plants, however, hybridization can be of central importance. In particular, for the genus Citrus, hybridization is a signal characteristic. Wikipedia provides an extreme but fair statement: 

All citrus trees belong to the single genus Citrus and remain almost entirely interfertile. This means that there is only one superspecies that includes grapefruits, lemons, limes, oranges, and various other types and hybrids.^[9] As the interfertility of oranges and other citrus has produced numerous hybrids, bud unions, and cultivars, their taxonomy is fairly controversial, confusing or inconsistent.

In short, any citrus plant can hybridize with many if not all other citrus plants. Combine this with the human nurturing that can keep any variety going, and the conclusion is that the notion of a genus and species as the way to uniquely identify an organism is lost. In standard evolutionary thinking, a species breeds true, so once you have assigned a genus and species name to an organism, you have nailed it. There is no further doubt about what it is. We are forced to abandon such certainty when it comes to citrus fruits. There are various substitute schemes for naming hybrids, but my view is that they don't really help, so I will not go into them. We are compelled to celebrate the uncertainty of citrus rather than dispel it.

In terms of a standard evolutionary tree, such as the one depicted above, as time passes, lineages split and die out in the manner of a tree branching over time. This assumes no hybridization, and once a lineage splits, it never comes back together. Once hybridization is allowed, however, loops appear in the diagram. We can still have a diagram, but it is no longer a tree, and species no longer stay distinct.

Something else to keep in mind is that two human parents can produce multiple children that all differ significantly. The same is true of plants. Two plants if mated repeatedly can produce offspring with very different characteristics, depending on exactly what mixture of genes is passed down to each descendant. This means that repeated hybridization events can produce very different offspring.

Citrus Evolution

Now it's time to put all this together into a coherent story of citrus evolution. This story, though based on a number of facts and on the best thinking I can find, still depends in part on conjecture. It should be thought of as conveying the flavor of what might have happened rather than being an exact and detailed description of what really happened.

It would be appealing to start with the basal citrus fruit from which all later citrus fruits evolved, but this basal citrus fruit in unkown to me.   Therefore, I will start somewhat later in time, when some evolution had occurred and produced what molecular studies show to be the four basal citrus fruits; this means that all citrus fruits are descended from these four fruits. Here is a list of these four basal citrus fruits along with the scientific name and the date of my e-mail on each.

• Papeda, Citrus hystrix (21 Mar 2015)
• Pomelo, Citrus maxima (19 Oct 2014)
• Mandarin, Citrus reticulata (7 Mar 2015)
• Citron, Citrus medica (14 Mar 2015)

My guess is that these four fruits existed by 10,000 BC and probably much earlier. The fruits of these names that we have today have probably evolved somewhat in the last 12,000 years, so, while close, they are not identical to the basal fruits.

A term that I need to introduce is "swarm." Biologists use "species swarm" to refer to a number of closely related species. I will use "swarm" to refer to closely related varieties. For example, consider the basal mandarin (7 Mar 2015) as it existed thousands of years ago. As time passed, mutations occurred to create different strains of mandarins. These strains hybridized, creating more strains, then more mutations occurred. Eventually, humans started breeding different strains, which created still more strains. The result is that now we have a swarm of descendants of the basal mandarins that are given names such as mandarins, clementines, tangerines, and satsumas. In this way, when hybridization readily occurs, swarms of closely related varieties come into existence. In short, our goal is not to specify for each citrus fruit its genus and species, which is a mugg's game, but rather to place each fruit into the proper swarm and to understand the genesis of each swarm. The picture below illustrates some of these swarms.

Another take on this theme is a picture taken in Hawaii by Mei-Mei earlier this year that shows the swarms of citrus fruits that grow on the Big Island. One surprise in this picture is that so many varieties of the pomelo are grown; the pomelos are the diagonal of big, greenish-yellow fruits close to the center of the picture. Another surprise is that the rootstocks are explicitly recognized; they are under the oranges toward the lower left.

Below is this e-mail's key diagram, which summarizes citrus evolution at a high level. It is modified from a diagram on a site that is devoted to rooting out botanical mistakes. The four basal citrus fruits are shown to the left of the dotted vertical line; the main citrus fruits currently extant are shown to the right. To indicate descent, an oval shows ancestors, and arrowheads point to descendants. The following events are shown. 

• The papeda and the pomelo hybridized to create the lime swarm (shown in brown).
• The pomelo gave rise to the current pomelo swarm (shown in blue).
• The pomelo and the mandarin hybridized to create the orange swarm (shown in green).
• The pomelo and the orange hybridized to create the grapefruit swarm (shown in yellow).
• The mandarin gave rise to the mandarin, clementine, tangerine swarm (shown in purple). 
• The citron and the orange hybridized to form the lemon swarm (shown in red). In particular, it is thought that the sour orange was the variety of orange that participated in this hybridization.

Note: Most of the information in this diagram can be found on various Wikipedia pages, but a better source is to use the Crop Search function on a Purdue site; Wikipedia often quotes verbatim from this site without attribution. Also, keep in mind that much of this is controversial; sometimes it seems like scientists can't agree on anything. I will not attempt a review of the competing theories. Moreover, be aware that much detail is omitted. Finally, the links to the various swarms given in the bullets preceding the diagram point to simplified lists of varieties; if you prefer excruciating detail, you can find it in book form or web format.

Note: Every hybridization event means that two branches come back together to form a loop in the diagram. The loop is not immediately apparent in this figure since the starting point of evolution at the basal citrus fruit is not shown in the diagram; it is off to the left somewhere.

Note: As for the kumquat, it is a matter of taste whether this fruit is placed in the genus Citrus or the genus Fortunella.  (See the discussion of splitters and lumpers in the e-mail of 24 Jul 2014). For this e-mail, the main point is that kumquats are clearly separated from the main line of citrus fruits that we are discussing, so it does not enter into the conversation.

Note: Now you can see why botanists (7 Mar 2015) use "mandarin" rather than "mandarin orange." The term "mandarin orange" implies that this fruit is one of the oranges, and the diagram clearly shows that this is not the case.

To avoid clutter, lesser hybridization events are not shown in this diagram. Standard disclaimer: There is controversy for many of these hypothesized hybrids.

• The tangerine and the pomelo hybridized to form the tangelo swarm (28 Feb 2015). It is thought that the tangelo originated about 3500 years ago.
• The orange and citron hybridized to form not only the lemon swarm but also bergamot. Bergamot is used in perfume (it was a major component of the original eau de Cologne in 18th century Germany) and to flavor Earl Grey tea. (To verify this Wikipedian statement, I ran over to Market Basket and looked at a package of Bigelow's Earl Grey tea. (I chose Bigelow's since it is a radio sponsor of the Red Sox. This proves that advertising works.) The only two listed ingredients were green tea and oil of bergamot. I then noticed another flavor of Bigelow's Earl Grey tea, and its ingredients were black tea and oil of bergamot. See the picture below of these two boxes of tea; if you look closely, you can see the ingredients on the right just below the center line. Apparently the essence of Earl Grey tea is not the type of tea but the bergamot. This seems mysterious to me, but then I don't care for tea and don't drink the stuff. You can see why I am not the tea explorer.) The experts say that the "t" in "bergamot" is pronounced. If you get fancy and drop the "t," the cognoscenti will snicker at you.
• The mandarin and the Ichang papeda (pictured in the e-mail of 21 Mar 2015) hybridized to form the yuzu (10 Apr 2015).
• According to some, grapefruit, sour orange, and tangerine hybridized to from the uniq (17 Jan 2014 and 27 Jan 2015).
• For other citrus fruits, you can google them, determine their ancestors,and figure out where they fit into the diagram. 

   

Of the four basal citrus fruits, the mandarin is the only sweet one, so we have the mandarins to thank for the sweetness of oranges. 

History of the Orange

Here is my conjectural interpretation of some of the key events in the history of the orange, the world's favorite citrus fruit. (I have also included events that concern the clementine and tangerine, which are near-oranges rather than an oranges.) Again, there is much controversy, which I only hint at below.

• The early history of the first orange, or sweet orange, is obscure. For  thousands of years mandarins and pomelos had grown in Southeast Asia. For some reason, they eventually hybridized. Maybe some climate change at the end of the Ice Age shifted their ranges so that this was the first time that their ranges overlapped. Maybe their ranges had long overlapped and the hybridization was just a lucky event. Maybe hybridization had occurred many times, but this time humans were there to nurture the hybrid. Keep in mind that it was after 10,000 BC that humans started to domesticate crops. At first there was unconscious domestication, in which humans gathered from the wild the more desirable fruits, took them home, ate them, discarded the seeds, and inadvertently grew the desirable fruits around their habitations.Some think that unconscious domestication of the  orange occurred in India around 7000 BC; some think in Southeast Asia around 4000 BC. One fact is that the orange is unknown in the wild state, so it is a reasonable conjecture that oranges persisted only because, consciously or unconsciously, humans nurtured them.
• The period of conscious domestication occurred at the latest in China sometime around 2500 BC. Orange orchards made their appearance on earth.
• Oranges were popular in China among the wealthy, and they flourished for thousands of years as a luxury good. As the centuries passed, there were opportunities for mutations, natural hybrids, and human breeding and management.
• The sour orange (21 Jul 2014) apparently appeared in Southeast Asia some time in the first millenium AD. Crusaders and traders brought the sour orange to Europe in the 11th century, and for hundreds of years thereafter it was the only orange in Europe. (There is plenty of controversy. One authority, p. 4, claims that the Romans were growing sour oranges by 100 A.D.) (In my e-mail of 17 Jul 2014 I was intolerant and had nothing but contempt for the sour orange, but now I can see its importance in the history of oranges and of lemons as well. Maria, in her comment of 21 Jul 2014, was much more measured and reasonable. I think there is a lesson here.)
• The sweet orange was brought to Europe by Portuguese traders around 1450 and the wealthy established orangeries to produce this new luxury..
• The blood orange (8 Feb 2015) is apparently a natural mutation that, according to one view, was discovered in Sicily in the fifteenth century.
• The navel orange, it is thought, originated between 1810 and 1820 as a single mutation in an orange tree near Bahia, Brazil. This event gave rise to all of the navel oranges (with the minor exception of a blood navel orange that was created by a second mutation).
• Humans had developed the art of grafting (1 Feb 2015) by the sixteenth century at the latest. Grafting has proved absolutely critical in orange horticulture, and without it the navel orange could not have persisted and oranges generally could not have been brought to the present level of productivity, consistency, and disease resistance. (Note added 3 Sep 2017: Grafting was known in ancient Rome as early as 300 B.C. Grafting is discussed in Pliny the Elder, Natural History: A Selection, Penguin paperback, 1991, p. 199.)
• The Jaffa orange or shamouti (4 Apr 2015) was first observed in 1844 as a mutation of a navel orange.
• The clementine (7 Mar 2015) was first observed circa 1900 as a hybrid between a mandarin and an ornamental citrus.
• The cara cara navel orange (8 Feb 2015) was discovered in 1976 as a mutation on a navel orange tree on the Hacienda Cara Cara in Valencia, Venezuela. 
• As the plasticity of the orange has become clear and as the size of the market for a better orange has become appreciated, breeding efforts have continued, intensified, and produced many varieties. The Sumo mandarin tangerine (28 Feb 2015) is a product of a targeted breeding effort that started in the 1970s and that sought to combine the ease of peeling of the tangerine with the taste of the orange. This orange has been developed in the last forty years and only became widely available in this country in 2012,

Closing Thought

My closing thought is that the citrus fruits are not a fixed group of fruits. Over the millenia this group of fruits has expanded with a stream of new varieties, many of which have been discussed in these e-mails, and the pace of change is accelerating. For example, the cara cara, my favorite citrus fruit, came into existence only in 1976. Moreover, the sumo mandarin tangerine, which bids fair to replace the cara cara as my favorite, only became available on the east coast in 2012. As time passes, we can expect that the creativity of nature and the tireless efforts of plant breeders will allow us to choose from an ever-growing selection of ever-improving fruits.

Acknowledgement

This e-mail has been written over a period of about two months, and during the writing I have profited greatly from numerous discussions with Mike Nienhaus.

Rick

P.S. A new Oiesen made the scene on Easter Sunday, 5 April 2015. Estevan Jan Oiesen-Vreeke is the son of my nephew Erik Oiesen-Vreeke and his wife Sonya. Estevan continues the family tradition of being born on a holiday; of my maternal grandmother's first four grandchildren, two were born on April Fools Day and one on Groundhog Day. Here is a picture of Estevan. Scale is provided by Erik.