Steinina ctenocephali

Cat fleas (Ctenocephalides felis) is a parasite that everyone would be familiar with one way or the other. It is found worldwide and is the bane of cats, cat owners and basically anyone who does not like getting their blood sucked by tiny insects. But cat fleas are themselves just another animal and are host to their own parasites, such as Steinina ctenocephali; a single-celled parasite that lives in the gut of cat fleas. In that sense I guess one can regard S. ctenocephali as a hyperparasite - a parasite that parasitise a parasite.

(A) Female cat flea infected with feeding stages of Steinina ctenocephali (indicated by white arrow heads), (B) Male cat flea infected with feeding stages of Steinina ctenocephali (indicated by white arrow heads), (C) Scanning electron micrograph (SEM) of the parasite's feeding stage, (D) SEM of oocysts infective stages in a flea's gut wall, (E) oocysts of the parasite as seen through a hematocytometer. [all photos from Fig. 1. of the paper)

Steinina ctenocephali belongs to a group of single-celled "protozoans" call gregarines. They are parasites of arthropod and other invertebrate animals, and despite being single-celled, they are comparatively large, with some species having cells that reach almost a millimetre in length. They also have some rather unusual shapes for a large single-celled organism, with some species shaped like worms and there's even a genus that looks kind of like a rubber chicken. Steinina ctenocephali is not nearly as oddly shaped those species - it is roughly pear-shaped, which is pretty generic for a gregarine. However, far more noteworthy is the way that this parasite has thoroughly integrated itself into the flea's life-cycle.

Fleas are holometabolous insects that undergoes complete metamorphosis. This means much like butterflies and wasps they have larval stage that looks radically different to the adult form.
Newly hatched baby fleas look somewhat like bristly worms with chewing mouth parts and they are not at all equipped for blood-sucking. So what do baby fleas eat? Until they become fully-fledged jumping vampires, they mostly feed on organic detritus - some of that include poop from the adult fleas, which also contain undigested blood.

Steinina ctenocephali uses this cycle of poop-eating and blood-sucking to infect each subsequent generations of cat fleas and propagate in the flea population. In the adult flea, S. ctenocephali attaches to the gut wall as a feeding stage, eventually producing infective spores called oocysts which are released into the environment with the flea's faeces. Then, along come the flea larvae that gobble them up and inoculating themselves with S. ctenocephali. In the flea larva, the parasite take up residence inside the cells, eventually moving into the gut tract when the flea metamorphose into an adult and take its first blood meal.

Being infected with parasites usually carry some kind of cost for the host, in fact that is the very definition of parasitism. But the paper being featured in this post reveals another side to this gregarine-flea interaction. For their study, the researchers obtained flea eggs from a captive colony and raised them in microwells filled with a type of powder which is kind of like baby food for fleas. When the larval fleas hatch, they feed on this powder mixture until they metamorphose into blood-sucking adults. For the experiments, half of the fleas were raised on powder which had S. ctenocephali oocysts mixed in, while the other half were raised on a parasite-free diet.

The researchers did not find any differences in the survival of infected and uninfected fleas, but there was a difference in their growth rate. Parasites usually divert resources away from the host itself, and by doing so reduce the hosts' growth rate. But instead of what one might have expected, the researchers found that fleas raised on food dosed with S. ctenocephali actually grew faster than their uninfected counterparts. The infected fleas became mature adults a few days earlier than uninfected fleas. In fact, the more parasites they've been dosed with, the faster they grew. On average uninfected fleas took about 19 days to reach adulthood, whereas fleas that got a high dose of S. ctenocephali took only 16 days to become adults.

The researchers suggested that this faster development could be due to hormonal manipulation on the part of this (hyper)parasite. The sooner the infected fleas become adult, the sooner it can start pooping S. ctenocephali spores that can go on to infect even more fleas. Alternatively, it could be some kind of compensatory growth response by the fleas, and the cost of this accelerated growth may manifest later in life in other ways (such as reduced egg production or immune function)

Given that S. ctenocephali seems to give its host a competitive edge (at least when it comes to reaching reproductive maturity earlier) over their uninfected counterparts, is it really a parasite? One thing to keep in mind is that parasitism is just a another type of symbiosis. Terms like parasitism, commensalism, and mutualism are just categories that we have come up to place such interactions into some kind of context which are more convenient for our own understanding. But nature does not care about our categories and all symbiotic relationships exist along a gradient - in the natural world the line between friends or foes is fuzzy and may change at any time.

Reference:
Alarcón, M. E., Jara-f, A., Briones, R. C., Dubey, A. K., & Slamovits, C. H. (2017). Gregarine infection accelerates larval development of the cat flea Ctenocephalides felis (Bouché). Parasitology 144: 419-425.