Honey and Bread: An Evolutionary Story

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Earlier this Spring I went to our department seminar which was given by the entomologist May Berenbaum. Berenbaum studies chemical interactions between plants and insects. I have known her work since my graduate school days, because my Ph.D. thesis was also about insect herbivores and plants (although I did not focus on the chemistry; my primary interest was how insects move through the landscapes so that they can find good plants to eat).

Why is chemistry important? Most non-biologists don’t realize that plants are constantly waging chemical warfare against most animals. There are zillions of animals that love eating plants, and plants really resent it. I can kind of relate to that, because my wife, who is an avid gardener, hates herbivores with a passion (especially when she finds in the morning that deer ate her favorite hostas).

Plants cannot take up a Kalashnikov and start shooting herbivores, but over the millions of years they’ve been evolving increasingly effective methods of protecting themselves against herbivory. The most effective way for them to fight back is by chemical warfare.

Tissues that plants want to protect are loaded with what ecologists call “secondary compounds.” To explain, primary compounds are those that have obvious functions in plant metabolism, such as capturing solar energy to produce carbohydrates. But when ecologists started studying the chemical composition of plant leafs, stems, seeds, etc., they found hundreds of chemicals that had no clear function. Later it turned out that most of these “secondary compounds” were toxins that plants used to protect themselves against depredations by herbivores.

Animals have to respond to this challenge (or they would starve), so over the millions of years they evolved elaborate ways to detoxify plant food. Insects have been particularly adept in these evolutionary games, because they have fast generations times, breed like, well, cockroaches, and, as a result, can rapidly evolve defenses against plant toxins.

cockroaches

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The whole spiral of offense and counter-offense is a classic example of an evolutionary arms race. Have you wondered why insects evolve pesticide resistance so easily? It’s because they have been contending against natural pesticides produced by plants, who want to protect themselves against herbivores. After tens of millions of years of the arms race against plants, insects find the pesticides we come up with pathetically easy to evolve to detoxify. Sure, when a new pesticide is introduced it can kill 99%, or even 99.99% of individual insects. But the better it works, the stronger selection pressure on the population it exerts, and the faster insects evolve ways to detoxify it.

We know a fair bit about the mechanisms of insecticide resistance. It turns out that insects have a family of proteins, known as CYPs, which they use to detoxify poisons.

These CYPs are quite amazing. One such enzyme, found in an insecticide-resistant Anopheles mosquito (that’s the one that transmits Malaria), is capable of directly metabolizing DDT.

Not everything that plants grow needs to be protected by secondary compounds. Some things plants actually want us to eat. This includes fruits and nectar. Which brings me back to the talk by May Berenbaum.

bee

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Her main topic was the honey bee. As some of you may know, our main source of honey, the European bee (Apis mellifera) is currently not doing so well. The problem is known as the colony collapse disorder (CCD).

The causes of CCD are not completely understood, and are likely to be complex, but Berenbaum’s conclusion was that the main culprit is pesticides. The problem is that over the last tens of millions of years honeybees have been eating a diet that was very low on, or even lacking toxins (remember, plants don’t want to poison bees, whom they need to transport their pollen to other plants). As a result, bees have been out of the chemical warfare arms race, and largely lost their capacity to deal with toxins. Today, with pesticide use so heavy, bees can’t help but pick pesticides up as they go about performing their key job of pollinating plants, including many of the commercial varieties. As the pesticide load accumulates, the colony may abruptly collapse.

Berenbaum showed a neat table, which I chased down to a publication by Fang Zhu et al. (2013) in BMC Genomics. This table shows that different insect species possess different numbers of CYPs.

Insect Number of CYPs
Pediculus humanus 38
Apis mellifera 48
Bombyx mori 84
Drosophila melanogaster 90
Tribolium castaneum 143
Insecticide-resistant Aedes aegypti 164
Insecticide-resistant Culex quinquefasciatus 204

The champions are the two insecticide resistant mosquitoes (Aedes and Culex), with 164 and 204 CYPs, respectively. It’s having these enzymes that enables them to thrive in insecticide-heavy environments. At the opposite end of the spectrum is the human louse (Pediculus humanus). The lice have only 38 CYPs, because their food source, human blood, is toxin-free. (CYPs can have other functions, which is why the number of them in a louse is not zero).

Now note the honeybee (Apis mellifera). With only 48 CYPs they are right next to the lice. That’s because their food is largely toxin-free.

The big surprise is the flour beetles (Tribolium castaneum). These guys eat flour, so what do they need a whopping 143 CYPs, for God’s sake?? Is flour nearly as toxin-laden as the pesticide-rich environment to which Aedes and Culex have adapted?

flour-beetle-1

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Those readers who have followed my posts on the post-Neolithic diet (aka Paleo diet) would not be surprised with the answer. Yes, the seeds of wheat, as well as other grasses, are literally loaded with natural pesticides, which the plants deposit to deter herbivores (including us) from eating them. In fact, the secondary compounds are so thick in a wheat seed, that it needs to metabolize most of them before sprouting.

flour

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So what does this evolutionary story tell us? Honey is a good food. Not only it is free of toxins, it has many compounds that actually promote health (which is why honey is used as an ingredient in many traditional medicines). If you have a sweet tooth, eat honey!

jar of honey with honeycomb on wooden table
jar of honey with honeycomb on wooden table

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Bread, unfortunately, is a completely different story. The only reason flour beetles can thrive on flour is because they have a truly remarkable number of CYPs to detoxify the wheat poisons. They acquired this detoxification system over many millions of years of evolution. Humans have nothing comparable to that. So stay away from bread!

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Francisco

Hello Peter, nice to read you again. According to the logic of the article, it seems to me we should abstain from eating any vegetables other than fruits. Where am I wrong, if so?

O.Voron

One more reason to enjoy honey and avoid wheat?:)

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