Chasing the Red Queen

The Evolutionary Race Between Agricultural Pests and Poisons

Andy Dyer

• Publisher: Island Press
• Year: 2014
• Print ISBN: 9781610915199, 9781610915182
• eBook ISBN: 9781610915205
• Topic: Sciences biologiques
• Subtopic: Écologie

In the race to feed the world's seven billion people, we are at a standstill. Over the past century, we have developed increasingly potent and sophisticated pesticides, yet in 2014, the average percentage of U.S. crops lost to agricultural pests was no less than in 1944. To use a metaphor the field of evolutionary biology borrowed from Alice in Wonderland, farmers must run ever faster to stay in the same place—i.e., produce the same yields.

With Chasing the Red Queen, Andy Dyer offers the first book to apply the Red Queen Hypothesis to agriculture. He illustrates that when selection pressure increases, species evolve in response, creating a never-ending, perpetually-escalating competition between predator (us) and prey (bugs and weeds). The result is farmers are caught in a vicious cycle of chemical dependence, stuck using increasingly dangerous and expensive toxics to beat back progressively resistant pests.

To break the cycle, we must learn the science behind it. Dyer examines one of the world's most pressing problems as a biological case study. He presents key concepts, from Darwin's principles of natural selection to genetic variation and adaptive phenotypes. Understanding the fundamentals of ecology and biology is the first step to "playing the Red Queen," and escaping her unwinnable race. The book's novel frame will help students, researchers, and policy-makers alike apply that knowledge to the critical task of achieving food security.

PART I

Introducing the Red Queen

In the game of life, less diversity means fewer options for change. Wild or domesticated, panda or pea, adaptation is the requirement for survival.

—Cary Fowler

Chapter 1

The Never-Ending Race: Adaptation and Environmental Stress

In the natural world as well as the business world, staying one step ahead is the key to success. However, it isn’t possible for everyone to stay one step ahead of everyone else. One is reminded of Garrison Keillor’s Lake Wobegon, where “all of the children are above average.” Clearly, it isn’t possible for everyone to win the race for success—and it is a race. In nature, regardless of the particular situation, those that fall behind become food for others. The Red Queen’s advice to Alice suggests to us that adapting to an ever-changing world is a continuous requirement for survival; being good isn’t enough, and we must work constantly to stay ahead of the pursuers . . . and the competitors . . . and the predators.

An analogy we can use is that of the fox, a predator, and rabbits, the fox’s prey. The fox pursues, the rabbits run. If the fox catches the slowest rabbits, then only the fastest rabbits remain in the population and their offspring (the next generation) should be faster than the average rabbit of the present generation. This is the basis for the phrase “survival of the fittest”: those individuals that are most “fit” in this environment are most likely to survive to reproduce.¹ However, as the prey population becomes faster and better able to avoid the predators, the predator population will die out unless it adapts to be fast enough to continue to catch the slower prey.² Hence, the faster and more successful foxes produce faster fox pups, while the slower foxes fail to survive or reproduce. Logically, this process of adaptation appears to be a positive feedback cycle. If the foxes are continually catching the slowest rabbits, the rabbit population will become faster and faster over time until we witness supersonic rabbits flashing around being chased by equally supersonic foxes. Obviously, this reductio ad absurdum result does not happen, and it is important to understand why.

First, there are limits to how fast a rabbit (or a fox) can run. Even if the genetic potential existed in the population, the energy requirements, the physiological demands, and the physical properties of the body all interact such that there are limits to the range of possible modifications. A supersonic rabbit would be all legs, with an incredibly high metabolism, and bones and sinews made of something unusually strong. Such a rabbit certainly wouldn’t eat grass.

Second, and more importantly, running faster isn’t the only solution to fox predation for the rabbits. Hiding, camouflage, mimicry, early detection, evasive action, changes in activity times, movement to predator-free habitats, claws and teeth, toxins, and group defense are all examples of adaptations used by animals to avoid or prevent predation. A population lacking adaptive options is a population that will soon run its course.

Regardless of the mechanism, the Red Queen demands that a population adapt or it will fall behind in the race for survival. Adapting isn’t optional; it is mandatory: adapt or go extinct. The fittest individuals survive, but the definition of “fittest” can change with every generation as the conditions change. Therefore, for every stress or challenge or demand in the environment, organisms that respond in an appropriate way are more likely to survive than those that do not respond appropriately. The challenges of the environment are many and varied and may not be the same from one year to the next, but the challenge to the individual is the same: meet the demands of the environment or become food for those that do.

Simply put, all adaptations are a response to environmental stress. A “stressor” can be thought of as any influence in the environment that lowers the ability of an individual in a population to survive and reproduce. An adaptation is a trait that reduces the negative effects of that stress. To be clear, adaptations do not eliminate stress; they only reduce the stress experienced by the individuals in that particular generation. Those individuals able to tolerate an environmental stress are more likely to live longer than those less tolerant, and as a result are more likely to produce more offspring. Therefore, the survival of a population or a species is a process of responding to stress, and because there are myriad different potential stressors in the environment, this process is constant and ongoing: it never ends. Nonetheless, however challenging survival may be to each individual in a population, it is only necessary to stay one step ahead of the pack. As the saying goes, when you’re being chased by a bear, you don’t have to run faster than the bear, just faster than the person next to you.

The premise of the Red Queen has been adopted by evolutionary biologists to exemplify the concept of continual adaptation to the constancy of environmental stress. Specifically, the Red Queen Hypothesis was originally used to understand the tight relationship that can evolve between a pathogen (or parasite) and its host. In such a situation, the pathogen must be successful at defending itself from the protective measures of the host, but the pathogen cannot be overly successful in a numerical sense or it will kill the host. If the host dies, the pathogen dies unless it can successfully transfer to a new host. Any host that can defend itself from the pathogen will be much more successful than those that can’t, but any pathogen that succumbs to the defensive measures of the host will be replaced by those that can resist. Thus, over the long term, a sort of détente evolves wherein pathogens are successful enough to persist and the hosts are successful enough not to die too quickly. In both cases, success can be measured as “lives long enough to reproduce”—or to infect another host, in the case of the pathogen. For both, their adaptations for survival allow the environmental stress to be reduced, but not eliminated, and the race goes on.

One critical component in this process is this: all adaptations are a function of time and this time is measured in generations. Ultimately, the only reason any species has ever become extinct is that the stress the species experienced was operating on a shorter time scale than the adaptive process could accommodate.³ The Irish elk, the largest deer that ever lived, did not die out because of an inability to adapt, but because the changes to the environment at the end of the last ice age occurred faster than the Irish elk could adapt to them.⁴ Obviously, this huge deer could and did adapt—males could be seven feet tall at the shoulders with twelve-foot-wide antlers—but the changes in the post-glacial environment of Europe and western Asia occurred more quickly than the giant deer could cope with. It is certainly possible that expanding human populations and their technology may have compounded the stress.

Similarly, the extinctions of the great auk, the passenger pigeon, and the sea mink did not occur because there are no possible adaptations to the activities of humans, but because the time needed for such adaptations is longer than the amount of time the species had available to them.⁵ The great auk, for example, was not able to tolerate the simultaneous stresses of human hunting and egg collecting. What was different about those stresses compared to those the great auk had faced for thousands of years prior? Do humans create greater stress than ice ages or polar bear predation?

The answers lie in an understanding of the principles of evolutionary biology. Those populations that can adapt quickly can stay one step ahead; they can successfully respond to the Red Queen’s admonition to “run faster.” The stronger and more intense the stressor, the faster the adaptive process must operate to reduce the stress and, consequently, the more likely it is that populations with slow adaptive responses will fail to adapt. Failing to adapt even once means extinction, and those species with slow response times are therefore more likely to become extinct. And it should come as no surprise that far more extinctions are seen in large organisms than in small organisms. Why are large organisms so slow to adapt? Why does it make any difference what the size of the organism is when it comes to responding to environmental stress? Why are there more insects than tigers?

As a general rule, when the individuals of a population encounter a new environmental stress, some individuals in the population will die prematurely and some individuals will survive. If the reason for their survival (such as a slightly enhanced ability or trait) can be passed on to their offspring (that is, it’s genetically encoded), then the next generation should be better able to withstand the newly encountered environmental stress, and the population overall will be less susceptible to it. Therefore, the first key to the ability of a population to survive by adaptation lies in the rapidity with which the next generation, the more resistant generation, is produced by the survivors of this generation. It follows that those species capable of producing a new generation very quickly should be better able to respond to a stress very quickly. Those species that require more time for reproduction will be slower to adapt to the stress because of the additional time needed for them to produce stress-tolerant offspring.

For example, consider three very different organisms: bacteria, houseflies, and elephants. A bacterium can reproduce every 20 minutes. A housefly may lay up to 500 eggs, and the offspring can be laying eggs of their own in as little as a week. Elephants can produce a baby every four years, and the offspring may require 10–15 years to mature to the point where they can produce a single baby of their own. One bacterium reproducing every 20 minutes can (potentially) produce 72 generations of ~5 x 10²¹ (5 sextillion) descendants in 24 hours. The offspring of one housefly can (potentially) produce four generations numbering 4 x 10⁹ (4 billion) individuals within a month. One elephant can (potentially) produce six young in 30 years. Using similar parameters, Charles Darwin calculated that elephants would need 750 years to produce 19 million individuals. Bacteria, houseflies, and elephants do not adapt at the same rate.

The production of large numbers of offspring is not a survival necessity, but high reproductive output is definitely correlated with the very short generation time that is critical to rapid adaptation. The housefly produces four generations in a month and those offspring can soon number in the billions. However, the fact that we are not (usually) overrun with houseflies indicates that organisms that reproduce at very high rates and in large numbers also experience very high mortality rates.

A second factor in survival via rapid adaptation to environmental stress is the size of the population. As a rule, the larger the population, the more likely the species will be able to cope with environmental stress because of the greater amount of genetic variation. A population of a billion houseflies is far more likely to contain a wider range of genetic variation and, therefore, of stress-tolerant individuals than a population of a hundred houseflies. And if those houseflies are descendants of a partly or wholly stress-tolerant individual, the alleles of the gene (see box 1-1) for that tolerance are likely to exist in large numbers, too. A contrasting but equally well-established principle in ecology is that physically large organisms have lower population densities than do smaller organisms. This general relationship, again, makes it more likely that smaller-bodied organisms, with rapid generation times and larger population sizes, have the greater capacity to adapt more quickly than large-bodied organisms.

A third factor controlling adaptation in organisms is that the intensity of the environmental stress will influence the rate at which the population can adapt. We assume that only a small proportion of a population is likely to be tolerant of a novel stress in the environment. If a low-intensity stress kills only a few individuals, the remaining population will comprise individuals across the entire range of tolerance. While the genetic variation within the population may have been reduced, the offspring in the next generation will still represent a wide range of genetic variation. However, if a high-intensity stress kills a large majority of the population, only the most tolerant individuals will remain. The resulting offspring will represent only the very narrow range of genetic variation that confers resistance to the environmental stress. Given a sufficiently intense stress, with all of the offspring being descendants of very tolerant survivors, adaptation could occur as quickly as one generation. The population will be small, but completely tolerant of the stress.

Box 1-1: All the genetics you’ll need

Throughout this book there will be references to the genetic makeup of individuals and populations. For now, consider all species to have two copies of each chromosome, just as humans do. One set is the maternal contribution and one set is the paternal contribution to their offspring. A specific chromosome contains a number of genes, and the genes are the DNA code for specific proteins. All individuals in a species possess the same genes, but each individual is likely to have different versions of many of those genes. These versions are called alleles. Your parents most likely gave you different alleles for each of the genes on each of your 23 different chromosomes. Only very closely related individuals are likely to have many of the same alleles.

When the two alleles are the same, an individual is homozygous for that gene, but heterozygous if the two alleles are different. A dominant allele will mask a recessive allele (in a heterozygous individual) and the expression of the recessive alleles will often only be seen when there are two copies in a homozygous individual. For example, in humans, albinism is the absence of pigmentation (melanin) and is a recessive trait only seen in individuals who have two copies of that allele. Heterozygotes with only one copy of the dominant allele appear normally pigmented because the dominant allele allows normal levels of melanin to be produced.

A change in the genetic code (DNA) of a normal allele results in a mutation. Mutations are random errors in the copying (transcription) of the DNA. (If a mutation in an important gene has a very negative effect, the individual will likely not survive and the mutation will be eliminated.) If mutations occur in sperm or egg cells, they can be passed on to the offspring that result from that particular sperm or egg. Most mutations have no strong effects, but some have a negative effect and a few will have a positive effect. In very large populations (say, a billion houseflies), there are almost certainly a large number of mutations present, and some of these may be positive and increase the survival chances of the possessors of the mutation. For a mutation to spread in a population, the environment must favor the possessor of the mutation in some way, and that advantage must lead to a relatively higher reproduction rate of that individual compared to the rest of the population.

Taken together, the interactions among reproduction rate, population size (and therefore genetic variation), and the intensity of stressors helps us to understand the response and survival of populations. A stress that kills a large majority of the in...

Table of contents

• Cover
• Title Page
• Copyright Page
• Contents
• Preface
• PART I: INTRODUCING THE RED QUEEN
• PART II: IGNORING THE RED QUEEN
• PART III: TRYING TO BEAT THE RED QUEEN
• PART IV: PLAYING THE RED QUEEN
• Notes
• Index