OCTOBER 15, 2014
IMAGINE an insecticide-soaked mattress crawling with bedbugs. You now have a metaphor for the future of our relationship to the living world. In the second half of the 20th century, synthetic pesticides all but eradicated the four-millimeter-long blood-sucking insects in the developed world. Today, those same poisons have little effect, and so, bedbugs have returned, lurking beneath mattresses and between bed frame slats — ready for dinner when we’re ready for sleep.
The case is no different for other bugs in our day-to-day life, as environmental toxicologist Emily Monosson details in Unnatural Selection: How We Are Changing Life, Gene By Gene (Island Press). Monosson surveys a world we have subjected to coordinated chemical warfare for the better part of a century, and finds life has evolved its way around our pesticides, antibiotics and chemotherapies.
Bedbugs are a particularly intimate example, at least from the human perspective, of the broader trend. Surveys of exterminators report that between 2001 and 2007, the number of bedbug infestations across North America increased 20-fold, concentrated in places like apartment complexes, college dormitories, and homeless shelters in major urban areas. Some of this resurgence is due to international travel. Major ports like New York, San Francisco, and Miami are epicenters of bedbug activity, and genetic surveys show that the bugs are arriving from multiple populations, not spreading from a single geographic source. Still, a large part of the bedbug revival is attributable to the fact that the bugs have developed a resistance to many of the insecticides that kept them down for decades.
This insecticide resistance is unquestionably genetic, and it is striking. In one study, entomologists at the University of Kentucky found that bugs from resistant populations in Cincinnati, Ohio, and Lexington, Kentucky, were at least 12,000 times as resistant to the insecticide deltamethrin as bugs from a laboratory colony that had never encountered insecticides. The resistant bugs were so resistant that the team was unable to determine a standard benchmark of deltamethrin toxicity — the LD50, or the dose that kills 50 percent of exposed bugs — because it would have required a higher concentration of the insecticide than can be dissolved in the delivery agent, acetone.
More recently, the same research group determined that the outer layer of resistant bugs’ integument — their skin, essentially — is modified at the molecular level to prevent deltamethrin from penetrating into deeper tissues where it has toxic effect. This particular form of insecticide resistance has not been seen in any other insect species, and it leaves us with much the same set of anti-bedbug tactics our pre-industrial ancestors used: steam-clean clothing, discard infested upholstery, sweep every nook and cranny, and beware of mattresses left curbside for the taking.
These insectival developments come as no surprise to evolutionary biologists. In Unnatural Selection, Monosson builds from the bedrock principles of natural selection that Charles Darwin and Alfred Russell Wallace first articulated more than a century and a half ago. Start with a population of living things that vary in some manner: color, running speed, ability to sniff out food, or capacity to withstand a toxin. If the variation in that trait determines which members of the population are able to survive and reproduce, and if the trait has a genetic basis that passes from parents to offspring, then the next generation will contain more individuals with the “favored” version of the trait. This process shaped the history of life over billions of years, eventually resulting in Homo sapiens, a species capable of synthesizing chemical compounds to eradicate other forms of life that cause us inconvenience.
Yet, as Monosson explains, our chemical conquest has never been as complete as we thought, especially outside the developed world. Antibiotics, pesticides, and herbicides, applied on a global scale, are exceptionally strong agents of selection. The lucky bacterial cell, or malarial mosquito, or agricultural weed that can carry on in an environment soaked with these agents has a tremendous advantage over its susceptible siblings, and in short order those mutants come to define a new, resistant normality.
The most widely known example is probably bacterial resistance to antibiotics, particularly in the wake of increasingly alarming statements from national and international health agencies, warning that we risk losing some of our most foundational medical treatments. Bacteria able to survive onslaughts of penicillin emerged within the first years of that early antibiotic’s widespread use; Alexander Fleming, who discovered the drug, famously warned of the dangers of resistance evolution in his speech accepting the Nobel Prize in medicine in 1945. This pattern has repeated itself with the development of each new antibiotic: as quickly as biochemists identify and synthesize new anti-bacterial compounds, bacteria evolve to overcome them.
Similarly, the introduction of the insecticide DDT rapidly led to the evolution of resistant mosquitoes, houseflies, and, yes, bedbugs. Decades of farming with the herbicide glyphosate, better known under the brand name Roundup, have led to the evolution of resistance in dozens of weed species. One after another, Monosson ticks off cases, dividing them into chapters corresponding roughly to biological classification. She goes beyond these headline examples to describe lesser-known triumphs of “resistance evolution,” such as viruses evading human immune responses and inadequate vaccination, cancer cells overcoming chemotherapy, and fish that survive water polluted by biochemical toxins. She opens most chapters by sketching the histories of particular treatments and pesticides, and explains genetic and biochemical technicalities in clear, precise prose.
Sometimes Monosson’s choices of personalizing detail are less than telling, but more often than not she delivers deft analogies. She compares recombination — how viruses exchange and mix genetic code — to two decks of differently colored cards, shuffled together. She also draws out the common themes across the many disparate organisms and environments she discusses. Resistance is more likely to evolve, she explains, when chemical agents are potent but incompletely applied, when the target population is large and variable, or when our synthetic pesticides are chemically similar to toxins that exist in the natural world, which pest populations may have already encountered.
So Unnatural Selection turns out to be a stealth lesson in basic biology — just the book to give to a friend or family member who thinks that evolution has little to do with day-to-day practicalities.Monosson’s focus on chemical toxins does mean, however, that sheskips many other classic examples of evolutionary responses precipitated by human actions. For example, plants growing on soils polluted by mining waste have repeatedly evolved the capacity to survive heavy metal contamination; species ranging from songbirds to butterflies to fruit flies and mosquitoes have changed the timing of their breeding seasons, or their temperature tolerance, in response to warming global climates.
Then, too, there are evolutionary changes humans have caused without even realizing it. In 2013, ornithologists Charles Brown and Mary Bomberger Brown reported 30 years’ worth of their observations of a colony of cliff swallows that built their mud-daubed nests on highway overpasses in southwestern Nebraska. Swallows hunting for insects over high-speed roads is a recipe for roadkill, but Brown and Brown found that the number of road-killed cliff swallows decreased steadily over their decades-long records. They also observed that swallows’ wings had become shorter over the same time period, and that swallows they found dead on the highway had longer wings than the general population. Long wings are well-suited for swift flight, but less so for rapid mid-air maneuvering, and Brown and Brown believe that selection by oncoming traffic has created shorter-winged cliff swallows that are better able to dodge a speeding sport utility vehicle.
Yet for all these evolutionary survival stories, there are myriad cases where evolution has failed to overcome humanity’s alteration of the world around us. The mounting list of species extinctions — there have been only five periods in the history of the planet with comparable losses of biological diversity — is a testimony to how often life has not found a way around our activities. In a recent review article for the journal Science, a team of evolutionary biologists led by Scott P. Carroll explicitly connect the basic principles of evolution in response to selection to sustainable global development goals. Their report divides evolutionary changes that complicate and threaten human lives, like insecticide and antibiotic resistance, from the much longer list of living systems that need to adapt, but cannot.
Carroll and his co-authors note that, in the course of tracing the origins of species, evolutionary biologists have developed experimental protocols, genetic analysis, and mathematical models that may be critical to minimizing the biological toll of climate change and other human alterations to the environment. With these tools, we can, maybe, identify species most threatened by environmental change, predict whether they will be able to adapt, and even choose genetic stocks to transplant from warmer parts of a species’ range in order to prepare northern populations for higher average temperatures. In the midst of the sixth global mass extinction, these efforts offer hope of some rescues, even if they cannot stop the flood of loss.
Toward the end of Unnatural Selection, Monosson addresses the question that arises naturally from her subject: if living things can evolve to cope with the ways we have changed the planet, why should we try to slow or undo those changes? Her answer is that “I worry not only about the species, but about individuals.” That is, although humanity as a whole may manage in an evolving world, failure to moderate our use of chemical agents will mean a future of real, individual people sickened by un-killable bacteria and left hungry by impervious agricultural pests. The same logic applies to the rest of the living world. Life, as a whole, will almost certainly survive the worst we can do to it — but how many varied and beautiful living creatures will be selected out of existence in the process?