6. The long-term outlook for pesticides

Can we win against crop pests? In a word, no. The reasons for that are many and rather inter-twined, but suffice it to say: our efforts to beat back the enemies of our crops only makes them stronger and the harder we try, the more quickly they win at the game. On the other hand, if we quit trying, they win easily. The rules of evolutionary biology dictate the outcome.

OK, is it possible for us to predict the emergence of resistant pests or the mutations that provide that resistance? Well, yes and no. First, if we persist in the use of chemical pesticides as our primary weapon against the multitudes of creatures that want to share our crops with us, there will be resistant pests and that means the mutations are present and are being favored. If that’s a form of “predicting”, then yes, we can predict the emergence of resistance. Can we know when and where the mutations for resistance will emerge? No. Are they going to emerge? Yes.

Let’s use the lottery as an analogy. The probability of any one person winning PowerBall is 1 in 175,000,000. In other words, my odds of winning are 0.000000006 which is the same as saying that if I bought 1,000,000,000 tickets, 6 of them would have the winning numbers. (The MegaMillions lottery is worse at about 4 chances in a billion.) So, my odds of winning are zero. How is it the odds of winning are zero, but someone always wins? Because as more and more tickets are sold, the odds of one of them having the winning numbers goes up. The odds of it being you or me are zero, but the chances of SOMEONE winning is quite good, if many millions of tickets are sold. This is also why the games tend to roll over several times before someone wins. Unfortunately, if the draw is truly random, there is no possibility of predicting in advance who the winner will be.

Now, in a field of insects eating lettuce and being assaulted by the latest pesticide, the odds of an individual possessing a random mutation conferring resistance to that pesticide are extremely small. But all individuals possess random mutations and in a field of millions of insects, the odds of one of those millions of mutations being just the right one for resistance to or tolerance of the pesticide is actually quite good. So, the odds of any insect possessing a favorable mutation (i.e., a winning lottery ticket) are essentially zero, but the odds of a favorable mutation existing are high. Indeed, if a pesticide is not particularly specific and kills a large number of different species, the odds of a mutation for resistance go up dramatically. That’s because we would be allowing a larger number of players in the game.

So what is the solution to the pest resistance problem? There is no solution- there are pests and there will always be pests because we have the defined the term “pest” as “those organisms eating plants we don’t want them to eat.” They aren’t inherently pests; they are extremely well-adapted organisms. For tens of thousands of generations, nature has selected the traits that allow these organisms to persist and thrive on certain plants. Every “pest” species out there is an example of nature shaping and molding a species to survive and reproduce regardless of the obstacles. To try to eliminate them is like trying to deny LIFE itself.

In every possible way, nature has designed organisms to succeed in the face of adversity. Evolutionary biology is the study of how nature has sculpted organisms to withstand environmental stresses and every species in existence has survived every stress it has ever faced. They are supremely well adapted to dealing with anything we can throw at them. Pesticide resistance isn’t a problem for nature, pesticide resistance is evidence of nature finding a solution to a problem. Fundamentally, pesticide resistance isn’t a failure of humans, it’s a success of nature.

Our attempts to control the species found in nature are a direct challenge to the evolutionary system. Our failures verify and validate the system, the rules of evolutionary biology, and nature’s ability to create organisms that can rise to meet any challenge. That makes our attempts to “control” the agents of nature just one more obstacle in the path. And our attempts at control using chemicals are blunt and crude in comparison to predators and pathogens that co-evolve as their prey species are pursued.

5. Pesticide Cross-Resistance

The concept of cross-resistance is well known in the medical world and in research on bacteria. The idea is that when a bacterial strain becomes resistant to one antibiotic, it can become resistant to another similar antibiotic even though the bacteria has never been exposed to the second antibiotic. Bacteria are the best organisms for investigating this sort of resistance and there is tremendous interest in understanding how bacterial evolution is capable of such a feat.

A report in the journal Nature Communications in July 2014 (doi:10.1038/ncomms5352) gave details on a study that tested E. coli exposed to 12 different antibiotics and then looked at genetic changes in response. Based on the data, the researchers created a cross-resistance network of interactions among the drugs in relation to the bacterial genetics. The network suggested some interesting conclusions. First, resistance to one antibiotic can lead to multidrug resistance and not necessarily among drugs that interact. Second, the evolution of resistance does not necessarily rely on new mutations, but can arise from a variety of genetic modifications. Taken together, the results suggest that cross-resistance is not a particularly unusual outcome and may even be predictable.

We see high levels of resistance to pesticides in insects and weeds in the world of agriculture. Can cross-resistance become a problem here also? It already has. Australia sheep ranchers depended on Lolium rigidum (rigid ryegrass) as a high quality forage. A great deal of effort went into developing better strains of Lolium in addition to strains that could withstand a farmer’s efforts to eliminate the weeds in the Lolium fields. When low wool prices forced many ranchers to shift to wheat farming, Lolium became a major weed of wheat fields. In many ways it was already adapted to the wheat fields having been a crop plant itself for so long. Worse, it rapidly became resistant to common herbicides and showed evidence of cross-resistance to new herbicides. Some strains of Lolium rigidum from Australia are now resistant to seven different categories of herbicides- more than any other common weed species in the world.

This wouldn’t be such an issue if it weren’t for the fact that no new categories (Modes of Action) of herbicides have been developed since 1998 and the current herbicide arsenal is rapidly losing its effectiveness as newly resistant weed species emerge. If a multi-resistant weed with cross-resistance potential becomes widespread, farming in many places could be at risk.

So cross resistance can emerge in one weed and in laboratory E coli. Is that a huge problem? Perhaps. In a report published in Dec. 2014, Randall Bendis and Rick Relyea at the University of Pittsburg suggest the problem may be more widespread. They looked at ponds near agricultural fields that used the common insecticide chlorpyrifos, an organophosphate introduced in 1965. Common aquatic invertebrates in the ponds showed resistance to the chemicals used on the field and the closer the ponds were to the fields the greater the resistance (2014, Environmental Toxicology and Chemistry). That such resistance should emerge in non-target species as a consequence of proximity to the chemical is not surprising and has even been predicted. But Bendis and Relyea reported at the Ecological Society of America meeting in Aug. 2014 that lab tests showed cross-resistance in these organisms to unrelated chemicals that they have not yet been exposed to in the field. The consequences of such developments are hard to predict, but one of their observations is that resistance and cross-resistance could have serious consequences for the control of these organisms in ecosystems.

The development of pesticide resistance is inevitable if the chemical is used intensively and across large regions. There are many ways to avoid this outcome. The first of which is to recognize that we continue to pursue chemical solutions to control problem organisms that are able to counter such chemical stress with ease. Now, we are faced with the fact that these organisms have even greater ability to resist our chemical attacks, abilities that we don’t understand but which we are facilitating with our actions.

The development of pesticide resistance is inevitable if the chemical is used intensively and across large regions. There are many ways to avoid this outcome. The first of which is to recognize that we continue to pursue chemical solutions to control problem organisms that are able to counter such chemical stress with ease. Now, we are faced with the fact that these organisms have even greater ability to resist our chemical attacks, abilities that we don’t understand but which we are facilitating with our actions.

4. The Value of Mutations

It’s common knowledge that genetic mutations are bad. Most SciFi and Horror movies will attest to that, but we also understand that a great deal of human suffering occurs because of genetic mutations and abnormalities. The huge number of deleterious alleles in the human genome is the result of mutations and when two of them match up in an embryo, it almost always results in problems. So, genetic mutations are bad.

The problem with pesticide resistance around the world is that insects and bacteria and all other nuisance species develop resistance as a direct result of mutations. When a toxin is first applied, the mortality rate in the target pest species is very close to 100%, but within a few years, sometimes less, the toxin eliminates a smaller and smaller percent of the pest population until eventually the person applying it is just wasting money (and likely polluting the environment for no good reason.) And it’s always because a mutation for resistance emerges and spreads through the population. Mutations thwart our efforts to control pest species. So, again, mutations are bad.

If we think of life as a process of adapting to the stresses of the environment, and those stresses change both regularly and unpredictably, there is a very basic need for genetic variation in any population. Without genetic variation, every individual would be identical and equally susceptible to every new stress. All genetic variation in all species comes from mutations; ultimately, there is no other source of genetic variation. And survival in the face of stress requires genetic variation. But wait, doesn’t that imply that mutations are good?

Consider humans facing a new and lethal bacterial threat, such as Yrsinia pestis, otherwise known as Bubonic Plague. In 1347-1351, the plague traveled from Mongolia, swept across the Mediterranean Basin and then devastated Europe. At least 28 million people died which was about 40% of the population. In large cities, the dead accumulated so rapidly the municipalities were incapable of handling the bodies and the dead were buried in mass graves. In rural areas, many small towns appeared afterward to be abandoned as everyone seemed to have died. That’s what the records tell us, but what they often fail to mention are underling reasons for the patterns of death. Yes, cities were hit first and the numbers of dead were staggering, and cities typically are where epidemics emerge. But the mortality rate in the cities was never 100% as it may have been in many small towns. Almost certainly the reason for that was genetic diversity.

Cities, especially ports, were and are melting pots where people from all over the region and perhaps the world mix. Diseases can be prevalent because of the high contact rates among so many people, but historical per capita death rates were lower due to the high genetic variation among all of those inhabitants. In contrast, small rural towns in medieval times were populated entirely by closely related families, clans, and groups who often maintained a high level of social isolation from other communities. Most had been born and raised in their town, they married and had children who followed suit. With the onset of a new and highly contagious epidemic, if one person was susceptible to it, then virtually every person was susceptible to it. The low genetic variation within the local populations meant the probability of resistance from a random mutation was very low.

Every species is capable of adapting to the stresses of the environment and no living species has ever failed to adapt. The capacity to adapt is the result of mutations that provide variation in the ability to respond to those stresses. Without mutations, nothing can survive the repeated attacks from nature. Humans, like any other species, have survived those attacks and that legacy is written in our DNA. Quite literally, if it weren’t for mutations, we would not be here today.

If survival is predicated on genetic variation, and genetic variation can only arise from mutations, then mutations are necessary for survival. And it should therefore come as no surprise that the insects we attack with pesticides answer the call to adapt so readily. And if mutations are that integral to survival, it is certainly possible that our attempts to eradicate our pests may favor future generations with even higher mutation rates.

Modern agriculture is predicated on the attack. Every chemical pesticide is an attempt to eradicate a species that has a very long history withstanding attacks. We have never eradicated a pest and we never will. In fact, our untiring efforts have only made them stronger and more capable. This is the basic message of Chasing the Red Queen.

3. It’s in the news every day

There are two concepts that are central to the problem of pest resistance in agriculture. One is that small organisms with rapid reproduction can adapt to the harshest of stresses in very short amounts of time. This is the basic underpinning to pesticide resistance everywhere. The flip side is that large organisms cannot adapt quickly because they require too much time to produce offspring. As a direct result, large-sized species are more likely to disappear locally when a severe stress occurs.

The reason this is so relevant is because pesticides are a severe stress. We see rapid evolution in response to pesticide stress in small organisms such as insects. And because large organisms, such as the predators of the small organisms, are much slower to evolve, they tend to disappear and then no biological controls are present to keep the pest species at bay.

A major review paper was just published in Science by Scott Carroll, Peter Jorgensen, and colleagues that focused on just this concept. (http://www.sciencemag.org/content/early/2014/09/10/science.1245993) (By the way, when Science gives this much space to a paper, they consider this a topic of the utmost importance and relevance to science and the public.) The overall point of the paper is that pathogens and pests species can adapt fast enough to keep pace with the changes humans impost on the environment, while many others species cannot. Their core concern is that this has major implications for medicine, agriculture, and the long-term stability of the world economy.

Their overall premise is that it all comes down to an understanding of evolutionary biology and such an understanding also provides avenues for developing solutions. In particular, Carroll and Jorgensen et al are proposing a broadly defined field of applied evolutionary biology that can direct our efforts to manipulate the genetic variation in organisms we favor, such as crop plants, and to do battle against the organisms we want to control, such as bacteria and crop pests. Let me say that for their ideas to come to fruition, we MUST assume that humans are part of the environment and have a long evolutionary history as members of the environment. Once we adopt that understanding into modern medicine, we can more rapidly align our living environment with the genetic history we all carry with us. For example, the western diet (described by Michael Pollan), with its very high proportion of processed carbohydrates, is absolutely contrary to the diet of our ancestors. Combine this with a more sedentary lifestyle and lifespans that are more than double what they were 100 years ago, and we have a desperate and growing medical situation with obesity, diabetes, auto-immune diseases, cardio-vascular diseases, cancer, and (yes!) infectious diseases. While Carroll and Jorgensen et al may not say so explicitly, I will: All of these problems of a highly technological, chemically-dependent, and environmentally destructive, urbanized society are linked. But they are not a necessary outcome.

I applaud Carroll and Jorgensen et al for their insights and thorough treatment of this subject and I hope this paper finds its way into the highest reaches of policy development. Of course, their discussion of agriculture and pest resistance is of great interest to me, but I have to voice a warning concerning their advice. While genetically-engineered crops show tremendous promise, it is always over the short term. They are not solutions; they are bandages applied to a growing environmental wound. No matter what solutions biotechnology is able to devise, they do not address the basic evolutionary problem that I address in the Red Queen and that Carroll and Jorgensen et al state in their opening sentences: Small organisms can adapt as fast as we apply selective stress to them. This will not change. There are rules that govern evolutionary biology and we cannot avoid them and we cannot change them.

All biotech “solutions” will ultimately fail because they attempt to stop a process that is the bedrock of biology. That process is evolution by natural selection. However, if we truly understand the process and apply that understanding such that those rules guide human endeavors and our interactions with nature, it may be possible to greatly reduce the growing number of issues we face in medicine and agriculture. For example, we understand that high genetic variation in large populations of insects provides the raw material for withstanding our attempts to eradicate them. We apparently fail to understand that we cannot and will not achieve eradication of pest species with chemicals. On the other hand, we have completely ignored the value of genetic variation for withstanding environmental stress when it comes to our own crops species. Insects win because of genetic variation. Our crops are losing because of the lack of genetic variation and it’s a lack that we have actively encouraged as we developed high-yield and transgenic crops.

Carroll and Jorgensen et al have provided a nice template for framing this discussion, but it is just the starting point.   My goal with Chasing the Red Queen is to make clear the rules that govern such a discussion and in a way that’s readable and accessible.

2. This book vs. a textbook

I’ve been asked by textbook publishers if I had an interest in writing a textbook, my answer was always an emphatic ‘no.’ I don’t even like textbooks and I try not to use them because, let’s face it, if I find them overly simplistic and dull, it’s not hard to understand why my students buy them but rarely read them. And education research is pretty clear: reading textbooks is one of the worst possible ways to actually learn something.

Introductory textbooks are superficial and attempt to cover every possible aspect of a topic, but without any depth. Relevance and appreciation comes from deeper understanding.  Instead, I find it works better to address a relevant topic with a good non-fiction book on the issue, and then use that as a way to discuss the science and biology behind it. One of my favorite books currently is Unquenchable by Robert Glennon (2009, Island Press, ISBN 9781597266390). I begin my environmental science class with this book to emphasize the absolute dependence of life on water, the complete orientation of human society around it, the consequences of having unclean and polluted water sources, and the numerous dangers we are facing with its increasing scarcity, and yet we barely recognize that there is a problem. If anything, Glennon’s presentation makes the situation sound worse.

Millions of people die each year around the world as a consequence of unclean and scarce water. In the US, 25% of our domestic water, the cleanest and most dependable municipal water on earth, is used to flush our toilets after we pee on it. Isn’t that more relevant?

Combine this with books on the environment, food, trash, and pollution such as World on the Edge (Lester Brown, 2011), Garbology (Edward Humes, 2013), Fast-Food Nation (Eric Schlosser, 2005) and films such as Waste Land (2010), Plagues and Pleasures on the Salton Sea (2004), Chasing Ice (2012), and Blue Gold (2008) and I have a way to grab the attention of my students and jump into great discussions on the science behind current issues.

1. Chasing a better understanding of the role of evolutionary biology in the human environment (which is not any different from the natural environment).

I had several reasons for writing this book. First, as a university professor, I need it for my own use. I spend the bulk of my time trying to explain concepts in ecology, evolution, and environmental science courses to biology majors and to non-biology majors. My classes are not packed with facts so much as they are spent discussing and learning the concepts governing how organisms live in the natural world. My students then do a fair amount of writing to convince me they can express those concepts in their own words. All of these concepts are linked and inter-related and talking about one necessarily means referring to the others. This book is an encapsulation of many of the major topics in my courses, but in what I hope is a logical sequence that ties many of them together.

Second, not everyone goes to college, but I think everyone needs to have a clear understanding of these concepts. This book is an attempt to present, in non-technical terms, the rules that govern food production and the difficult situation in which we find ourselves nationally and globally.

Third, a large number of people directly and indirectly associated with farming and food production may benefit from a clear understanding of why they feel trapped in an increasingly complex system that should be and used to be relatively easy. I’m hoping a relatively jargon-free and non-technical book will help.