Genomics Uncovers How Insect Pests Crept Across the World

As night falls and the city bustle dies down, another kind of life creeps up on its citizens: Cockroaches lurk beneath cabinets and bed bugs crawl out of mattresses. These unwelcome guests have spread and thrived in the cracks of settlements all over the world, keeping up with human chemicals, architecture, and behaviors.

“Indoor urban pests seem to be these perfect model systems that [have] been around with us, sometimes for thousands of years, sometimes for millions of years,” said Warren Booth, an entomologist at Virginia Polytechnic Institute and State University. “We can really look at how humans and urbanization have really impacted their evolution.”

To do so, Booth and his team collect cockroaches and bed bugs during pest control treatments or from museum exhibits. They then use a variety of genomic methods to understand how the pests invade and spread in urban areas. They also investigate how the insects develop and evolve insecticide resistance, which could guide the development of better pest control strategies.

How Insects Evolved to Pester Humans Around the World

Ancient humans abandoned their nomadic lifestyles to settle down in colonies around 10,000 years ago, creating conditions—including access to food and dark, dingy corners—ideal for pesky insects.¹ Researchers found that bed bugs evolved millions of years ago, prompting Booth and his team to investigate whether the bugs plagued ancient humans as they started building permanent settlements.²

The researchers studied the genomes of two genetically distinct bed bug lineages: one that feeds on bats and one that switched to feeding on humans about 245,000 years ago.³ Comparing mutations in these lineages and modeling their populations revealed that human-associated bed bug numbers spiked about 13,000 years ago and then again 7,000 years ago.⁴

These timelines coincide with the periods when humans first began settling in colonies and then established bigger cities in western Asia, suggesting that bed bugs could have been the world’s first urban pest. “[When] the first civilizations hit, the environment was perfect for [the bed bugs], and they just took off,” said Booth.

In contrast, when the researchers analyzed the genomes of German cockroaches—the world’s most prevalent cockroach pests—from 17 countries, they found that these insects only evolved 2,100 years ago.⁵ “To find a species that is globally dispersed, that is one of the most significant indoor pest insects on the planet, and find out that it only became a species about 2,100 years ago. It's remarkable,” said Booth. “In that time, it spread across the globe, and it did it really fast.”

Genomic analyses helped the researchers trace how the species travelled to different parts of the world. The insects, despite their name, originated in India or Myanmar and hitchhiked westward with soldiers traveling to the Middle East. The cockroaches later spread towards the east with European colonial commercial activities.

Understanding Insecticide Resistance

These pests did not just spread across the world; they also evolved resistance to chemicals designed to kill them. “We've only been bombarding insects with insecticides for about 100 years, maybe even less than that,” said Booth. “And yet, in that time, many of these species that are associated with humans…have evolved numerous strategies to evade control.”

Comparing the genomes of bed bugs sampled from 2005 until 2019, Booth and his team discovered that the latter carried insecticide resistance-associated mutations more frequently.⁶ The genotypes of these insects did not show any signs of being susceptible to pesticides, suggesting that the persistent use of insecticides over a few years drove the bugs to adapt.

The researchers also compared the genes of bed bugs collected over 14 years and found the first evidence of a mutation that is known to confer insecticide resistance in other pests in the more recent samples.⁷ “It's remarkable how these species very rapidly evolved resistance,” said Booth, who also works with insecticide companies to help them design better pest control strategies.

Revealing the Genetic Secrets of Insects

Booth and other researchers usually sequence targeted genes or genomic regions associated with insecticide resistance to study it. Investigating how the insects spread and formed associations with humans in urban areas requires slightly different approaches because the researchers don’t know exactly which genomic regions are involved in this behavior. So, they compared the patterns of microsatellites—short, repetitive mutation-prone DNA segments—between different samples of insects. With advances in next-generation sequencing methods, researchers can now sequence entire insect genomes. “The whole landscape about how we work has changed dramatically,” said Booth, admitting that he looks forward to seeing where the field of urban entomology goes.

Despite covering a fraction of the earth’s surface, urban areas house over 55 percent of the world’s population, and experts estimate this number will increase further. “We impart all of these selection pressures on these organisms in urban environments, and now we can study, using genomics, how they're coping, how they're evolving within that,” said Booth. “That part is pretty exciting in regards to urban evolution.”