We often consider evolution a thing of the past. In reality, it may be occurring right under our noses, and perhaps even in our basements.
The year is 1941. Hundreds of Londoners, seeking shelter from the Blitz, gather in the London Underground. Families huddle together for warmth, children cry, and couples embrace as the musty air settles into their clothes. The explosions outside are muffled, but every sound triggers anxious glances. Even here, people don’t feel safe.
Not only do they feel unsafe, they just don’t feel comfortable. Red spots keep appearing on wrists, ankles and faces, and now and then someone hears a soft buzzing noise zooming past their ear.
Molestus, indeed. This mosquito caused enough annoyance during World War II to warrant such a name. The species is persistent, and even the bombshells above the London Underground didn’t bother them in the slightest.
Naturalist Petrus Forskal first described Culex molestus in 1775 from specimens collected in Egypt. However, the species entered the public eye during World War II when civilians were forced to share the London Underground with it.
Living up to its name, the London Underground Mosquito is only known to inhabit underground train systems, basements, and drainage and sewer systems throughout the world.
Its subterranean habitat makes it a huge curiosity, but its evolutionary history is even more mysterious. How could a species manage to inhabit all of these underground, man-made regions of the globe? Is it an instance of convergent evolution in every region where C. molestus occurs? This seems unlikely. The truth is that we don’t understand the evolutionary history of C. molestus at all.
“Interestingly, there is ongoing debate about whether this mosquito is a species or a 'biotype',” explains Cameron Webb, a medical entomologist from University of Sydney. “Taxonomists often have trouble telling specimens of Culex molestus and Culex pipiens apart.”
Despite their morphological similarities, these two closely related species differ in their habitat choice and behaviour. C. molestus is distinguished by its preference for underground habitats and its higher propensity for biting humans.
C. pipiens is thought to have evolved in tropical regions of Africa, later moving north into Europe’s cooler climates. It is likely that C. molestus diverged from this species and has since migrated to other continents by following the movements of humans. More work is required, however, to fully map out the species’ evolutionary history.
What we can gather is that C. molestus is an extraordinary example of recent speciation ‒ an instance of evolution that has occurred over hundreds of years, rather than thousands or millions. It has evolved during our time, alongside our own civilisations. As we’ve moved through the French and American Revolutions, the Napoleonic Wars and the two Great Wars, this species’ ancestors have been plodding along with us, gradually moving into our basements and waste systems.
It is very easy for us to forget that evolution is not simply a thing of the past. The buzzwords of “evolution” and “natural selection” conjure up images of Charles Darwin, fossils, and that human evolution poster plastered all over the Internet. We hardly ever think of evolution as something happening within our own lifetimes.
While the major dramatic changes we associate with evolution do gradually arise over thousands or millions of years, subtler alterations can occur over centuries or even decades. The presence and degree of change simply depends on the force of natural selection acting on a species at a particular time.
In 2003, University of Denver's Robin Tinghitella and colleagues were surveying oceanic field crickets (Teleogryllus oceanicus) on the Hawaiian island of Kauai.
“To locate cricket populations, we used to drive around the Hawaiian Islands slowly with the car windows rolled down, listening for the tell-tale song that male T. oceanicus produce,” says Dr Tinghitella. “[But] it was strangely quiet – no one was singing.”
The researchers feared that the cricket was locally extinct.
“As a last ditch effort,” says Dr Tinghitella, “we got out of the car and decided to search by foot. And the crickets were everywhere!”
Once the crickets were examined in the lab, it became clear that males had undergone a morphological change: their wings were feminised.
“The large forewings of male crickets normally boast a complicated 'instrument' that produces sound when males rub them together,” explains Nathan Bailey from St Andrews University. “There is a long, bumpy vein on the underside of one wing that plucks at a thickened edge of the opposite wing, and when that happens the whole wing vibrates, including specialised structures that quiver like the surface of a drum and produce sound.”
The feminised Hawaiian male crickets, called flatwings, either lacked or had reduced versions of these morphological ‘crinkled’ wing structures that create their song. They simply couldn’t sing anymore.
Miraculously, this alteration had occurred in just over a decade; long-term records suggest that these flatwing crickets didn’t exist in the late 1990s.
It seems completely counter-intuitive for the male crickets to have lost this ability. Without it, they drastically reduce their chances of attracting a mate. So why has this change occurred so rapidly?
It turns out that, while the crickets’ singing was attracting their female counterparts, it was also attracting a less amiable neighbour. The parasitoid fly Ormia ochracea locates crickets through hearing their song and deposits its larvae onto them. The larvae burrow into the crickets’ bodies and later consume them from the inside out. Clearly, avoiding this fate was a definite plus for the crickets.
Genetically, the rapid change was possible due to the wing morphology responding to a single mutation on a sex chromosome. The process was undoubtedly assisted, however, by the cricket species residing in an island setting.
We often see islands providing the perfect environment for rapid evolutionary change, but why is this the case? What is it about an island that creates such a natural laboratory for evolutionary biologists?
“There are many reasons,” Dr Bailey explains. “Some have to do with colonising individuals being subjected to new selection pressures, the potential for adaptive radiations into unoccupied niches, bottlenecks, and otherwise changed population dynamics.”
“Island populations are usually relatively isolated,” adds Dr Tinghitella, “and they can be small.
“Together, these characteristics mean that new mutations in island populations can spread really quickly – much more quickly than they would in large populations that constantly receive gene flow (immigrants) from neighbouring locations.”
The presence of small and isolated populations on islands and archipelagos creates hotbeds for evolutionary change. Not only can evolution happen in fast-forward, but the resulting speciation can also produce animals found nowhere else in the world.
The Galapagos Islands and Darwin’s finches have been a hallmark of evolution since Darwin himself. In 1947, David Lack specifically singled out the three Camarhynchus species, or Floreana Island finches, as a classic example of speciation through natural selection.
The Floreana Island finch species include the small tree finch (C. parvulus), medium tree finch (C. pauper) and large tree finch (C. psittacula).
“The tree finches descended from the shared ancestor for the Darwin’s finch radiation within the last 1.5 million years,” explains Sonia Kleindorfer from Flinders University. “Therefore, the Darwin’s finch radiation is considered the most recent and most rapid for any terrestrial vertebrate.”
Despite this history, Prof Kleindorfer and her colleagues’ recent work shows that Floreana finches are actually currently undergoing “evolution in reverse”. They are merging back into a hybridised species. Indeed, the large tree finch may now be extinct due to hybridisation with the other Floreana Island species.
Prof Kleindorfer’s team had been collecting DNA samples from Floreana Island since 2004.
“Our team discovered hybridisation in the tree finches in 2011,” she explains. “When we analysed the Floreana data in 2011 and 2012, we identified two genetic clusters and one group with ‘mixed assignment’. The birds with ‘mixed assignment’ were the hybrids.”
This hybridisation was likely due to mating between female medium tree finches and male small tree finches. Since the medium tree finch is critically endangered, females may simply prefer mating with higher quality males from the small finch species rather than within the limited pool of their own species.
In addition, all of Darwin’s finches are threatened by an introduced parasitic fly, Philornis downsii. Over 90% of chicks die annually as a result of the P. downsii larvae eating them alive in their nests.
The chicks that survive this turmoil are often left with enlarged holes in their beaks that negatively impact their song quality once they mature. The medium tree finch is most affected by this parasite, leaving the already limited line-up of potential mates unable to impress females with their song.
The Floreana finches are not only an example of speedy and recent evolutionary change, but their hybridisation complicates the very idea of what a species is.
“The term ‘species’ is shorthand for a biological cut-off that describes most patterns of gene flow between populations,” explains Prof Kleindorfer. “If there is no gene flow between populations that occur in sympatry [in the same geographic area], then we generally refer to these two groups as ‘species’.
“Hybridisation is the result of gene flow between two sympatric populations that had previously been described as not having gene flow. Therefore, hybridisation blurs the species boundaries.”
Since its introduction in 1935, the cane toad (Rhinella marina) has made itself infamous by spreading throughout Northern Australia. The toad’s increasingly rapid spread is a result of similarly rapid toad evolution.
“The interesting thing about cane toads is that, as they’ve spread through Australia, they have evolved to become more highly dispersive,” explains Ben Phillips from University of Melbourne.
“The animals that end up on the invasion front in every generation have to be the individuals that have moved the furthest – that is the only way they can be there – so the most dispersive individuals of the population are in the same place at the same time so they tend to mate with each other.”
This phenomenon, termed the “Olympic Village effect”, is a prime example of assortative mating, in which individuals of similar genotypes or phenotypes mate with each other. In this case, highly dispersive toads are mating with other highly dispersive toads and so their offspring are more likely to have high dispersal ability. Much like islands, the edge of the toad invasion front has created the perfect environment for rapid evolutionary change.
Not only has the cane toad evolved rapidly since its introduction to Australia, but native predators have been forced to adapt to the toad as it arrives in their environment.
Many of these predators, including goannas, snakes, quolls and planigales, are accustomed to eating Australian frogs, so toads initially appear to be just another tasty addition to their menu. Unfortunately, cane toads carry toxins called bufadienolides in two glands on either side of their bodies, and most Australian predators are not resistant to these toxins.
Just a small amount of the toxin can cause death in the largest of our native species. Even saltwater crocodiles are affected, and populations of the northern quoll and the red-bellied black snake have all but completely disappeared.
The immensity of the toad’s impact presents a strong selective pressure on native populations.
“The primary evolutionary force is on prey preference,” explains Dr Phillips. “So individuals that recognise toads are inedible, for whatever reason, or are capable of learning very rapidly that toads are dangerous, are much more likely to survive and reproduce.”
Conditioned taste-aversion learning has been used with quolls, planigales and goannas to discourage them from eating cane toads when they arrive in their habitat. Some native populations, however, appear to have evolved avoidance tactics without human assistance.
Dr Phillips and his colleagues are currently working on transferring this adaptive ability to quoll populations that have yet to experience the toad’s wrath.
“We’re trying to capture those toad-smart genes into naïve populations of quolls across Northern Australia. So we’re actually in the process of trying to speed up evolution through genetic translocation.”
The toad was released into Australia in 1935, only 80 years ago – a blink of an eye in evolutionary terms. However, as Dr Phillips points out:
“You have to remember that the timescale that evolution plays out on is one of generations. So many of the predator species, and certainly the toads, have a generation time of around a year, so eighty years is eighty generations – so it’s actually a very long time, but it’s still quite dramatic.”
From the Australian outback, to the Hawaiian Islands and the London Underground, evolution is rumbling on beneath our feet and right under our noses. We are constantly discovering instances of change occurring more rapidly than we ever thought naturally possible.
Adaptation, speciation and hybridisation are occurring due to the environments we create, the pests we release, and the ongoing interactions of predators, prey and parasites. While habitats and species are falling around humanity’s feet, it’s easy to forget the awesome power of evolution by natural selection. As with C. molestus, all that’s required are the right selection pressures.
“Mosquitoes are incredibly adaptive creatures,” says Dr Webb. “They probably deserve more of our respect.
“There are few aquatic habitats on the planet that haven’t been exploited by mosquitoes so it makes perfect sense that a mosquito would exploit the underground habitats we create, ranging in size from septic tanks to subways.
“This is probably what happened with Culex molestus; it found an unoccupied niche and decided to move in.”