Most mosquitoes bite a range of animals, but only a few of the 3,500 mosquito species around the world have evolved to prefer humans. These are the mosquitoes that have become dangerous vectors of infectious disease. Aedes aegypti is a good example, which is responsible for spreading Zika, dengue, yellow fever, and chikungunya in various regions around the world. Although A. aegypti currently inhabits many cities around the world, it originated as a forest-dwelling species in Africa. A group of researchers sought to understand how this transition happened and, more specifically, how the mosquito evolved a preference for human hosts.

The researchers from Princeton University identified two major factors: a dry climate and city life. Based on these findings, they predict that increased urbanization in the coming decades will mean even more human-biting mosquitoes in the future.

“Many people have speculated about why this species evolved to selectively bite humans, but our study is the first to address this question directly with systematic empirical data,” said Lindy McBride, PhD, assistant professor in ecology and evolutionary biology at the Lewis-Sigler Institute for Integrative Genomics of Princeton University.

The work is published in the article, “Climate and Urbanization Drive Mosquito Preference for Humans” in Current Biology.

A. aegypti mosquitoes are invasive across the global tropics, where a strong preference for human hosts and habitats makes them important disease vectors,” said McBride. “We found that in their native range of sub-Saharan Africa, they show extremely variable attraction to human hosts, ranging from strong preference for humans to strong preference for non-human animals.”

To do this, the researchers took advantage of the fact that this species came from Africa and that many populations in Africa still don’t like to bite humans. They asked a simple question: where specifically do the mosquitoes like humans? And, where do they prefer to bite other animals instead?

The researchers used traps to collect A. aegypti eggs from multiple outdoor sites in each of 27 locations across sub-Saharan Africa. They established 50 mosquito colonies from these samples.

They then tested the preferences of each of those mosquito populations for the scent of people versus other animals, including guinea pigs and quail, using a two post olfactometer which allows them to measure the olfactory preferences of the mosquitoes. Most mosquitoes were animal preferring, but a few showed a preference for humans. It was mosquitoes living in dense urban cities that were attracted to people more than those from more rural or wild places.

“Mosquitoes living near dense human populations in cities such as Kumasi, Ghana, or Ouagadougou, Burkina Faso, showed increased willingness to bite human hosts,” noted Noah Rose, PhD, a postdoctoral fellow in the McBride lab. “But they only evolve a strong preference for human hosts in places with intense dry seasons—in particular, in the Sahel region, where rainfall is concentrated in just a couple months out of the year. We think this is because mosquitoes in these climates are especially dependent on humans and human water storage for their life cycle.”

The researchers noted that this only applied to especially dense modern cities and therefore isn’t likely to be the original reason that certain population of A. aegypti mosquitoes evolved to specialize in biting humans.

They also found that climate had an effect. And, that it was bigger than that seen with urbanization. Mosquitoes living in places with longer and hotter dry seasons showed a strong preference for a human versus animal scent.

This image shows the kinds of human water storage containers where Aedes aegypti larvae thrive in areas with intense dry seasons and little natural habitat. [Noah H. Rose]

“When we took a more regional view of things, we saw that regions with dense human populations had mosquitoes with a greater attraction to human hosts, but this wasn’t dependent on the precise habitat we collected them from within each region,” Rose noted. “I was also surprised that climate was more important than urbanization in explaining present day behavioral variation. Many mosquitoes living in fairly dense cities don’t particularly prefer to bite human hosts.”

“I think it will be surprising to people that in many cities in Africa, this species actively discriminates against humans,” McBride said. “It is only when the cities become extremely dense or are located in places with more intense dry seasons that they become more interested in biting humans.”

Answers in the genes 

In order to understand the genomic basis of this behavioral shift, the team studied 345 unrelated genomes at 15x coverage in collaboration with the Verily-led 1200 genomes project. They looked at population structure and found three clusters: East African, West African, and a globally invasive human specialist cluster.

The researchers showed that many genes concentrated in a few key parts of the genome drove this evolutionary shift in mosquitoes’ biting preferences. Based on their findings, the researchers asked how near-term climate change and urban growth are expected to shape mosquito behavior in the near future.

The researchers say that climate change in the next few decades isn’t expected to drive major changes to the dry season dynamics they found were important to mosquitoes. But, they say, rapid urbanization could push more mosquitoes to bite humans in many cities across sub-Saharan Africa over the next 30 years.

The researchers will continue to study the interplay between mosquitoes’ biting preferences, climate, and urban life. They’d also like to understand why mosquitoes specialize on certain hosts to begin with and which specific genes and genetic changes are most important.

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