With almost every aspect of their biology and anatomy adapted to their specialised parasitic lifestyle, the fleas have long troubled evolutionary biologists.

From their peculiarly flattened bodies to their odd siphonate mouthparts, fleas are some of the most bizarre insects alive. Yet the unusual anatomy that made the group successful parasites of birds and mammals has also puzzled generations of zoologists. Even despite sequencing the first flea genomes in the last decade, their early evolution and position on the insect tree of life has remained a mystery. Now, a new study by researchers from the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (NIGPAS) in China and the University of Bristol in the UK promises to resolve this long-standing evolutionary riddle.

"Of all the parasites in the animal kingdom, fleas hold a pre-eminent position. After all, the Black Death, caused by a flea-transmitted bacterium, was the deadliest pandemic in the recorded history of mankind; it claimed the lives of possibly up to 200 million people in the 14th century. Yet despite their medical significance, the placement of fleas on the tree of life represents one of the most persistent enigmas in the evolution of insects," says Erik Tihelka, undergraduate at the University of Bristol who led the new study published in Palaeoentomology.

Over the course of the years, researchers have proposed many hypotheses regarding the origin of fleas, most arguing that their closest relatives lie among the flies or scorpionflies, or both. Now, scientists used genome-scale sequences of fleas and all their possible close relatives, and analysed them using new statistical methods. By using more sophisticated algorithms to test all historically proposed hypotheses and search for new potential relationships, the team has come to an unexpected conclusion – fleas are a group of highly modified, parasitic scorpionflies.

Scorpionflies are a group of small- to medium-sized flying insects distributed worldwide. About 600 species are currently known. The new study suggests that the small scorpionfly family Nannochoristidae endemic to the southern hemisphere whose adults probably feed on nectar is the closest relative of all living fleas. Despite looking very unlike the flea we know today, the Nannochoristidae in fact share surprising anatomical similarities with fleas such as characters of the head and the sperm pump.

Why did the "flea mystery" remain so hard to resolve for so long?

"A close relationship between Nannochoristidae and the fleas has been proposed in several past molecular analyses but was treated as likely an error. Ancient evolutionary radiations leave behind subtle clues in organisms’ genomes that can only be recovered with sophisticated models of molecular evolution. Moreover, the nannochoristids are a quite rare and little-studied group that only occurs in New Zealand, southeastern Australia, Tasmania, and Chile, so they are easy to overlook." explains Tihelka.

"The new results suggest that we may need to revise our entomology textbooks. Fleas no longer deserve the status of a separate insect order, but should actually be classified within the scorpionflies," says Prof. CAI Chenyang, a professor from NIGPAS and expert on Mesozoic insects.

The new findings agree with fossil evidence. "We have exceptionally preserved fossil fleas from the Jurassic and Cretaceous. In particular, some Jurassic fleas from China, about 165 million years old, are truly giant and measure up to two centimetres. They may have fed on dinosaurs, but that is exceedingly difficult to tell. What is more interesting is that these ancient fleas share important characters with modern scorpionflies," says CAI.

"Sometime between the Permian and Jurassic, a group of scorpionflies started feeding on the blood of vertebrates. This group gave rise to the fleas as we know them today," adds Diying Huang, professor of invertebrate palaeontology at NIGPAS.

"It is interesting.", comments Mattia Giacomelli, a PhD student at the University of Bristol who participated in the study. "We used to think that all blood-feeding parasitic insects basically started off by either being predators or living in close association with their vertebrate hosts, like in their nests. The case of fleas shows that blood feeding can evolve in groups that originally fed on nectar and other plant secretions. It seems that the elongate mouthparts that are specialized for nectar feeding from flowers can become co-opted during the course evolution to enable sucking blood." 

Reference: Erik Tihelka, Mattia Giacomelli, Diying Huang, Davide Pisani, Philip C. J. Donoghue, Chenyang Cai* (2020) Fleas are parasitic scorpionflies. Palaeoentomology 3(6): 641–653.

Contact:   

LIU Yun, Propagandist 

Email: yunliu@nigpas.ac.cn  

Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences  

Nanjing, Jiangsu 210008, China