Terrestrial fleas descended from plant-sucking scorpionflies to dine on ascendant amniotes. Tiny aquatic crustaceans begat water fleas.
Amniotes are the clade of tetrapod (4-limbed) vertebrates that beget both reptiles and mammals. They emerged over 312 million years ago.
Among the prominent evolutionary innovations of amniotes was dealing with desiccation, beginning with laying their eggs on land rather than in water. This was perhaps the greatest divergence from the amphibians that amniotes descended from.
Insects emerged roughly 500 million years ago, after land plants began to proliferate and habitats stabilized. Scorpionflies evolved elongate mouthparts to feed on sap, and later, nectar.
Amniotes presented another potential food source. Scorpionfly mouthparts which had specialized for floral fluids retuned to piercing tough hides. Digestive systems adjusted to consuming blood. Whence fleas.
Fleas on land had aquatic equivalents. Water fleas arose during the Permian from tiny crustaceans.
Like sharks, water fleas emerged with a near-ideal set of traits, including agile adaptability to survive significant ecological shifts. Their basic biomechanics have scarcely evolved since their arrival ~260 million years ago, while diversifying into over 700 species that occupy almost all freshwater environments.
When conditions are favorable, female water fleas reproduce asexually. Conversely, when environmental conditions deteriorate and variety becomes critical, males are produced and sex becomes the norm. This conditional reproductive system is known as cyclical parthenogenesis.
Though water fleas have various defense mechanisms to escape predators, some decided on a tamer domain: in groundwater. No longer needing sight, these subterranean crustaceans economically went blind and lost their eyes.
Back on land. As dinosaurs became behemoths, the fleas that preyed on them also upsized: to 10 times the size of the modern flea.
After dinosaurs died out, fleas downsized. In the process they acquired the strong spring-legged jump that lets modern fleas leap 100 times their height.
During dinosaur times, fleas had to scurry and hop on their prey. Alternately, ambush-style, they may have dropped from vegetation.
Modernizing fleas also adapted to suck blood without causing so much pain, thereby allowing getting a full meal without unduly agitating its host. This involved going from a jaw with saw-like projections to smooth mouth parts.
Ishi Nobu, “Dinosaur fleas,” in The Elements of Evolution (2019).
Ishi Nobu, “Water fleas,” in The Elements of Evolution (2019).
Erik Tihelka et al, “Fleas are parasitic scorpionflies,” Palaeoentomology (2020).