Aphids, apples and evolution

ResearchBlogging.orgWhy do some trees have red leaves in autumn? Yellow leaves are easy to explain; the breakdown of chlorophyll exposes yellow carotenoids that were there all along but masked. Red, however, is the result of anthocyanins, which the plant manufactures specifically. That imposes a cost, so evolutionary biologists have long looked for the corresponding benefit. One theory is that the red pigments protect the leaf from damage by light, especially at low temperatures, giving the tree more time to absorb and store nutrients from the leaves it is about to drop. Evidence on that is contradictory and inconclusive. Another is that the red pigment is actually a signal to insects or some other creatures that make use of the trees.

Turns out that the second is correct. Over-wintering aphids avoid trees with red leaves and do worse in the spring if forced to grow on those trees.

Marco Archetti, late of Oxford University and now at Harvard, has a paper1 that is forehead-smitingly clear and convincing, which is of additional interest here because it uses agricultural biodiversity, field genebanks and wild relatives as the natural experiments with which to test the hypothesis.

200904241459.jpg First off, aphids do avoid red-leaved trees. Archetti counted the number of Dysaphis plantaginea, which commonly lays eggs on apple to overwinter, on trees at Brogdale, the UK’s apple field genebank . Red-leaved varieties attracted fewer aphids than green-leaved varieties, which in turn were less attractive than yellow-leaved varieties. Of course, it might be that aphids just don’t see red leaves all that well. Perhaps the red leaves, noticeable though they are to us, are effectively camouflaged. To test this Archetti placed virgin female aphids in cages on the fresh green leaves of Brogdale varieties that had been planted three years previously at a nearby community orchard. Then he waited to see how many produced the winged adults that disperse in the summer. On red-leaved varieties, 29% of the females produced winged adults. On green- and yellow-leaved varieties (which did not differ) almost 60% of the females produced winged adults. Aphids are not as fit on red-leaved trees.

So it looks like the coevolution explanation has a lot going for it. Apple trees make red pigments that signal to aphids that the tree is a less than desirable host. Those aphids that do select red-leaved trees don’t do as well in the spring as those that avoid red-leaved trees. Without knowing exactly what it is about the host that leaf colour signals, we can see that the tree selects against aphids that choose it.

As Archetti drily observes:

The ideal test of the coevolution hypothesis would be to let populations of the same species evolve with and without insect pests for many generations: if autumn colours are a signal to insects, we would expect red coloration to be lost in the populations evolving without insects. This experiment would take too long to perform, but a similar test was actually initiated ca 2000 years ago with the domestication of fruit trees.

A trip to Central Asia is clearly in order. Among wild apple populations in Kyrgystan and Kazakhstan, in excess of 60% of the trees have red leaves in autumn. At Brogdale, just 2.8% of the 2170 cultivars2 have red leaves in autumn. And, pleasingly, cultivated varieties in Central Asia also tend not to produce red leaves; 39% turn red in autumn. There’s a similar pattern at other field collections around the world, so the loss of red colouration under domestication is not simply a reflection of growing conditions.

Why are red-leaved trees signalling? Theory suggests that are either more vigorous (and so can afford the signal) or are equally vigorous but have a greater need to avoid aphids. The US national apple collection has evaluated the vigour of trees on a standard rootstock. Red-leaved varieties do not differ from green- or yellow-leaved ones.

Why might trees need to avoid insects? Sap-suckers like aphids are known to transmit diseases, perhaps the most devastating of which is fire blight. And lo! US cultivars that turn red in autumn are much, much more susceptible to fire blight, suggesting that being red protects them from fire blight by keeping aphids away. (Varieties from Central Asia are highly resistant to fire blight, regardless of leaf colour, perhaps because fire blight originated in the US and has not yet adapted to wilder types.)

That’s almost the whole story. The final points are that red-leaved cultivars have smaller fruits than green- and yellow-leaved types. Archetti interprets this as an indication of less efficient selection: “Because increasing fruit size has been the main selective pressure under domestication, varieties that have undergone less efficient selection are expected to have smaller fruits.” Fruits described as “astringent” are also more common among varieties that turn red, and Central Asian varieties in the US genebank are more astringent than green- and yellow-leaved varieties, but no different from red-leaved varieties. “Since apple varieties have been selected against astringent flavour, this also supports the idea that cultivars with red leaves are more similar on average to their wild ancestors.”

And there you have it. Red leaves coevolved with disease-spreading insects because

(i) Aphids are more abundant on green and yellow autumn leaves than on red leaves.
(ii) Aphids have higher fitness in spring on trees with green and yellow autumn leaves than on trees with red leaves.
(iii) Autumn colours are common in wild varieties but rare under domestication.
(iv) Only varieties with high susceptibility to fire blight have red autumn leaves.
(v) Varieties with red autumn leaves have smaller fruits and more astringent taste.

Best yet, these conclusions make similar predictions for other domesticated trees, for example apricot and walnut that turn colour in the fruit forests of Central Asia but not in orchards of domesticated cultivars. Different pests and diseases are almost certainly involved, but the selective pressures remain the same.

  1. Archetti, M. (2009). Evidence from the domestication of apple for the maintenance of autumn colours by coevolution Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2009.0355 []
  2. Why does the Brogdale site list only 1893? []

What constitutes a “better” tomato?

Two recent blog posts sandwich a very unappetising slice of nonsense at Scientific American, and goad Jeremy into action.

Amy Goldman’s slideshow of heirloom tomatoes, hosted at Scientific American, prompted a little reverie for me. Unfortunately another linked Scientific American article by Brendan Borrell — How to Grow a Better Tomato: The Case against Heirloom Tomatoes — brought me back to reality with a start. It wasn’t easy to determine exactly what the article was about. It seemed to be be saying that all heirloom tomatoes are pretty much useless; toothsome yes, but disease-prone, weak, wimpy, and generally pretty useless. And gardeners who like and grow them are deluding themselves.

On the contrary, I find Borrell’s arguments to be weak, wimpy and generally useless.

Why describe heirlooms as having “fanciful” names? Aren’t Santa and Sungold pretty fanciful? Or are we supposed to feel that Aunt Gertie’s Gold and Green Zebra are quaint and old-fashioned and therefore ripe for discarding as we thrust forward into the bright new future? Funnily enough, Borrell doesn’t actually name any non-heirloom varieties. He restricts himself to identifying “run-of-the-mill hybrid varieties such as beefsteak, cherry and plum”.Those are not names, they are categories. New Girl is a name. Lemon Boy is a name. Viva Italia is a name. Not at all fanciful?

Describing heirloom names as “fanciful” is really a rather minor pecadillo compared to other points in Borrell’s article, but it does indicate where he’s coming from.1 He is determined to paint open-pollinated varieties in the worst possible light, in order then to blow a big fanfare for a spiffy new tomato that is the outcome of a “pet project” by breeder Doug Heath at Seminis Vegetable Seeds, a subsidiary of Monsanto.

The “new rainbow-streaked tomato [is] less prone to cracking and also endowed with 12 disease-resistant genes”. I expect it will find a ready market among commercial growers. Perhaps in addition to the 12 resistance genes it also has the sturdiness that industrial operations require. And those operations will be able to jump aboard the heirloom bandwagon and fool some of the people some of the time.

But why is it necessary to dump on heirlooms and backgarden varieties to make the point that Monsanto has bred what may be an interesting tomato? And why did Heath’s efforts to breed his tomato have to be a “pet project”? Sounds to me like Monsanto wasn’t initially all that interested in it as a commercial concern, but tolerated Heath’s efforts. And then, when there seemed to be an opportunity to ape heirlooms, in they stepped, encouraged no doubt by the fact that because the new heirloom is a hybrid rather than open pollinated, their investment in Heath’s pet project could be protected. And gushing, uncritical writers could be relied upon to puff their product.

Good luck to Monsanto, and let the buyer of pseudo-heirlooms beware. There need be no inherent conflict between F1 hybrids and open pollinated varieties, and many enthusiastic farmers and gardeners find no substitute for some F1s, such as Sungold. Borrell asks, “But will heirloom adherents appreciate the look-alikes with hybrid seeds?” He almost answers his own question with a final quote from breeder Doug Heath: “There will be a contingent of people who will believe these are poor imitations of the originals.” That, like Borrell’s entire article, misses the point.

The Extreme Gardener puts it well:

“I do not care to have Monsanto deciding for me what constitutes a better tomato, and I certainly don’t want to have to buy seed from them every season in order to grow tomatoes. We grow all the tomatoes we eat all year, and have very specific needs and preferences that may not be relevant to anyone else. Our varieties are adapted to us and our garden in our little corner of the planet.”

But it ought not to be a question of either or, at least not in countries where trade in seeds is reasonably free. The needs of gardeners and small farmers are different from those of industrial agriculture, and the two sectors ought to be able to coexist side by side. There isn’t much commercial interest in meeting the needs of small farmers and gardeners, but that may change.

The day before Scientific American published its article on Monsanto’s pseudo-heirloom, Gary at Muck and Mystery happened to resurrect a discussion of approaches to breeding. He raised (from the dead?) the notion of apomixis, once hailed as the saviour of developing country poor farmers. Apomictic plants produce viable seeds without crossing. The seeds are effectively clones. That means farmers can have all the benefits of wonderful traits incorporated into apomictic seeds for them by breeders without paying the penalty associated with hybrid seeds, which require them to obtain fresh seed each season. With apomictic seeds, farmers can simply save a portion of this year’s harvest for next year’s sowing. Breeders concerned with the public good were racing to incorporate apomixis into crops where it had never been. Then everything went quiet.

But hang on. Isn’t this where agriculture started, with farmers saving seed from one harvest to sow for the following season’s? Ah, but that was dumb breeding, characterized by both Gary and Scientific American as the kind of harmful breeding “that has lost many useful characteristics in the pursuit of others”. Smart breeding uses genomic information to make precisely targeted changes to the genome. The fact is, it is the smart breeders who have lost the useful characteristics. They are the ones who have created crop varieties in which every individual is identical to every other individual. And it is that uniformity that makes modern farmers reach for the pesticides and forces breeders to return endlessly to the genepool.

I have absolutely nothing against uniform varieties, honest, so long as we realize that thanks to the adaptability of their enemies and their own enforced stasis, they inevitably contain the seeds of their own downfall. And I don’t see myself as among either the “emo activists longing for a mythical past (with iPods)” or the “singulatarians longing for rapture,” as Gary describes them. But I do agree with him when he forecasts that “it will be the large ag businesses that will make the best use of genomics”.

Interestingly, the Wired article that Gary quotes so favourably, raises two points that he takes for granted, or at least chooses to ignore. One is that the methods of smart breeding will be “unpatentable”. Maybe so, but I am willing to bet that large ag businesses will find ways to protect their investment. The other point is that “nearly every crop in the world has a corresponding gene bank consisting of the seeds of thousands of wild and domesticated relatives”. Right. And who supports the genebanks? Not, so far, the large ag businesses that Gary and Wired agree benefit from them.

The suppliers to industrial ag, among them Monsanto, will deliver the products of their smart breeding programmes, particularly if they can exercise the property rights they need to make the R&D investment pay. That’s fine for industrial agriculture. It may also suit some consumers. But lets not fool ourselves. Those varieties will be no good for poor farmers or home gardeners, they won’t feed the world, and they won’t be sustainable.

My point is this: in plant breeding, as in plants, we need diversity. If you can afford to pay for the inputs that genetic divesity supplies for free, then by all means do so. But if you cannot, or don’t want to, if you want to use genetic diversity instead to cope with pests and diseases or climate change or drought or floods, then what? Setting up a false dichotomy between smart breeding and dumb breeding helps nobody. But people do need help, and they won’t be getting it from breeders intent on uniformity.

  1. I could bang on about the others, but it would serve no purpose here. []

Blogging the big birthday: Beans and selection

Given that he wrote an entire book on The Variation of Animals and Plants Under Domestication, Charles Darwin offers us a rich seam to mine.1 I was particularly struck by a phrase I thought I heard Professor Steve Jones use in the recent special series of In Our Time on BBC Radio 4, when he referred to Darwin’s garden at Down House as, I think, the Galapagos of Bromley. His point was that Darwin’s experimental work and observations in his garden informed his ideas no less than his journey.

There is a good deal in The Variation … about how plants change in their characteristics, from presumed differences among the maize varieties of New England and Canada to the northward progress by “thirty leagues” of the northern limit to growing maize in Europe, over a period of about 60 years. “[I]n Sweden,” Darwin writes, “tobacco raised from home-grown seed ripens its seed a month sooner and is less liable to miscarry than plants raised from foreign seed.”

These, and many others, are typical of the observations of others that Darwin accumulated and scrupulously credited. But he made his own observations too.

On the same day of the month [24 May], but in the year 1864, there was a severe frost in Kent, and two rows of scarlet-runners (P. multiflorus2) in my garden, containing 390 plants of the same age and equally exposed, were all blackened and killed except about a dozen plants. In an adjoining row of “Fulmer’s dwarf bean” (P. vulgaris), one single plant escaped. A still more severe frost occurred four days afterwards, and of the dozen plants which had previously escaped only three survived; these were not taller or more vigorous than the other young plants, but they escaped completely, with not even the tips of their leaves browned. It was impossible to behold these three plants, with their blackened, withered, and dead brethren all round them, and not see at a glance that they differed widely in constitutional power of resisting frost.

Darwin doesn’t there make the point that the survivors of such a killing frost might give rise to more frost-hardy offspring in due course. And I have not been able to discover whether he asked his gardeners to save seeds from those that had survived. I like to think he did. In The Origin (p 142) he very clearly anticipated such an experiment:

[U]ntil some one will sow, during a score of generations, his kidney-beans so early that a very large proportion are destroyed by frost, and then collect seed from the few survivors, with care to prevent accidental crosses, and then again get seed from these seedlings, with the same precautions, the experiment cannot be said to have been even tried. Nor let it be supposed that no differences in the constitution of seedling kidney-beans ever appear, for an account has been published how much more hardy some seedlings appeared to be than others.

This last may be a reference to a sharp frost on the night of May 24th, 1836, near Salisbury, when “all the French beans (Phaseolus vulgaris) in a bed were killed except about one in thirty”.

There is much, much more in The Variation … to amuse and instruct anyone with an interest in agricultural biodiversity. What I find odd is that despite the prevalence of seed saving in mid-Victorian England, Darwin was not able to prove to his own satisfaction that the beans of his own era were in fact hardier than those of previous times. Today’s scientifically informed seed savers ought to find it easy. Have they?

  1. Made easier by the existence of Darwin online. []
  2. These days Phaseolus coccineus. []

Chu-mar-tus-iz: Th. Jefferson and the Tomato

At last, I found my copy of The Tomato in America, by Andrew F. Smith. He is The Man on the tomato (and much else) in US history. I can thus enlighten myself (and Jacob) further on Thomas Jefferson and the Tomato. Smith writes:

51x3pj1xxtl_bo2204203200_pisitb-sticker-arrow-clicktopright35-76_aa240_sh20_ou01_ Despite the tomato’s presence along the Atlantic Seaboard and the Gulf Coast, its introduction and adoption in the interior areas of southern states appear to have been delayed. In Salem, North Carolina, tomatoes were not sown until 1833, when a gentleman from South Carolina sent seeds to an “old Mr. Holland.” At that time no one had tasted tomatoes, and scarcely any one had heard of them. Similar late arrivals were probably common for other rural areas of the South. In 1820 Phineas Thornton published a thorough inventory of the kitchen garden plants within a twenty-mile radius of Camden, South Carolina, and made no mention of the tomato. His Southern Gardener and Receipt Book, published twenty years later, included instructions for cultivating and preparing tomatoes for the table, which suggests that they were introduced in Camden sometime between 1820 and 1840.

Concurrently, as tomato culture expanded in the Carolinas, it also evolved in Virginia. According to Thomas J. Randolph, his grandfather, Thomas Jefferson, asserted that when he was young, tomatoes ornamented flower gardens and were deemed poisonous. By the account of J. Augustin Smith, president of the College of William and Mary, Jefferson met Dr. John de Sequeyra while he was in Williamsburg. Sequeyra had immigrated to America around 1745 and “was of the opinion that a person who should eat a sufficient abundance of these apples, would never die.” As he lived to old age, an unusual feat in the marshy environs of Williamsburg, his peculiar constitution supposedly resisted the tomato’s deleterious effects. This anecdote was published during Jefferson’s lifetime, which offers some credibility on its behalf. Sequeyra’s preoccupation with tomatoes was supported by other sources. E. Randolph Braxton reported that “Dr. Secarri,” his grandfather’s physician, “introduced the custom of eating tomatoes, until then considered more of a flower than a vegetable.”

Despite Sequeyra’s introduction, it is unlikely that tomatoes were grown extensively in mid-eighteenth-century Virginia. America’s first gardening work, John Randolph’s Treatise on Gardening, written in Williamsburg probably before the American Revolution, made no mention of them. A correspondent in the Farmer’s Register expounded that tomatoes were hardly ever eaten in Virginia during the 1780s and 1790s. He also explained that Virginians had called them love apples out of ignorance of their proper “foreign title, tomato,” which they pronounced as if it were spelt “chu-mar-tus-iz.” While Jefferson was in Paris in the 1780s he sent tomato seeds to Robert Rutherford, who grew and devoured tomatoes in Berkeley County in western Virginia. By 1800 Rutherford had convinced only one other person to eat them.

During the early nineteenth century tomato culture increased. While he was president, Jefferson noted that fresh tomatoes were sold in markets in Washington. They were sold in Alexandria by 1806, which suggests that they were used for culinary purposes by at least some residents. In 1814 they were eaten in Harpers Ferry. In the same year, John James ate them in a public inn near the Natural Bridge in western Virginia. The proprietor claimed that tomatoes had been used as an article of diet in that section as long as she could recollect. Thomas Jefferson grew them at Monticello beginning in 1809 and ten years later served them to Salma Hale.1 According to Hale, Jefferson claimed to have introduced them into America from Europe. If Hale’s recollection was accurate, Jefferson may have been referring to a particular variety of tomato, such as those sent to Robert Rutherford. By the early 1820s they were raised in abundance throughout Virginia and adjoining states and were regarded as a great luxury.

On Smith’s say-so, then, I believe one can discount all claims that Jefferson grew such and such a tomato in the 1780s and probably the 1790s too. But stories that add years to varieties have a powerful attraction, and if they are mistaken in detail, they also make the larger point. That the stories in which varieties are embedded are a signal of their importance.

  1. My emphasis. []

Where do your garden seeds come from?

Patrick over at Bifurcated Carrots had a post a couple of days ago echoing the “fact” that “98% of the worlds seeds come from one of six companies.” He went on to list them and to say a bit about how companies that sell smaller quantities have to enter into straightjacket contracts with the big six that mean the “small” guys cannot say where they get their seeds, or whether they are F1 hybrids.

I’m deeply skeptical of the original claim, and asked Patrick where it came from and how it was calculated. He replied:

This in not a very hard statistic. It originally came from the book Animal, Vegetable, Miracle. … I don’t own a copy of the book, and I have only seen lots of other people on the Internet cite the reference, so I can’t say a lot about it. I assume it does include cereal grains. I’m sure the person who came up with the statistic did it for purposes of making a point, rather than making an accurate statement. Perhaps this was a poor choice of a statistic to give here. If you have other ideas of a more accurate statistic, I’d love to hear.

On the final point, I have ideas, but not the ability to implement them. It is interesting, though, that there are far more than six registered maintainers of seeds listed in the EU Common Catalogue. But that’s an arcane discussion for another time. As for the rest, I had already determined that almost all the noise around this 98% number did trace back to Barbara Kingsolver’s book, and I do have a copy, which I’ve almost finished reading.

First, I had to find the quote. Not so easy when there is no index.1 But there it is, on page 51 of my US paperback edition, published by Harper Perennial. So I turned to the notes and references at the back of the book, to see if I could discover where Kingsolver had got the figure. Alas, the references given are not tied to anything; not the chapters, not the pages, certainly not the individual claims.

OK, I’ll just ask her directly. But can I find an email, or any other way to get in touch? Can I heck. Neither on her “personal web site” nor on the book’s site is there any way that I can see to get in touch with the author.

Shouldn’t I just give her the benefit of the doubt? After all, her heart is in the right place. Well, as I read the book I was making notes of inaccuracies and outright errors.2 I stopped because it was interfering with my reading and enjoyment, having to pause and find my notebook and pencil every page or so.

But this figure of 98% and six companies is gaining truthiness just by being echoed uncritically all over the shop, like so many other useful but wrong “facts”. It is a perfect example of what the great J.B.S. Haldane called The Bellman’s Theorem,3 and I fear that I cannot just ignore it.

There is concentration in the seed industry. There may be contractual obligations on people who retail seed from others. But people who think that those things are bad should not rely on untruths to support their arguments. My hope, then, is that while Barbara Kingsolver may not want anyone disturbing the quiet of her old Virginia home, she may just be egotistical enough to monitor, and care, what the internet is saying about her, and that she’ll pop up in the comments here to tell us all where she found the figure, so that we can go back and check it for ourselves.

That’s how one assesses truth.

  1. There is one now that you can download from the book web site. []
  2. Sample: page 57, Arugula is not, and never has been, a member of “the lettuce clan”. []
  3. “What I tell you three times is true.” []