Parvatrema spp.

Parasites are known for their complex life cycles, especially among parasitic flatworms such as flukes. And the flukes that are being featured in today's post have life cycles that make them a fluke among flukes. This blog post is about an extensive study that culminated from 25 years of work, where a group of researchers were able to identify and describe five different fluke species with a peculiar life cycle adaptation.

Parvatrema sp. “quadriramis” cercaria stage (left), young metacercaria (centre), parthenogenetic metacercaria containing fully-formed metacercariae (right). Insert: Parvtrema parthenogenetic metacercariae in the hepatopancreas of a limpet.
Photos from Fig. 4 and Fig. 11 of the paper

In the cold waters of the northern European seas and the Sea of Okhotsk, there is a group of parasites with life cycles that defy the conventions of its class. They are five closely related species of flukes in the genus Parvatrema, and they spend parts of their lives lurking quietly in the bodies of clams and snails. In many ways, they're just like other digenean flukes, with multi-host life cycles that involve turning their first mollusc host into a clone factory, producing clonal larvae which go off to infect a second host, and culminating in sexually mature adults living in the gut of vertebrate animals. But these Parvatrema flukes have evolved to do some things differently once they reach their second host.

These flukes infect sea snails such as limpets and periwinkles as their second host. Some species sit in the extrapallial space - the fluid-filled gap between the snail's fleshy mantle and the shell, others get into the gonads and digestive organs. Usually, this is a relatively dormant stage of the fluke life cycle, where they literally sit and wait to be swallowed by the appropriate final host. But with these Parvatrema flukes, instead of simply sitting around waiting to be eaten by a bird like other flukes would, they have another round of asexual reproduction, as a treat.

Each of those immature flukes become filled with numerous miniature clones of itself until it is stuffed to the point of exploding. Some of them take it further, with unlimited consecutive generations of parthenogenetic clones, each fluke exploding into multiple clones and then each of those clones explodes into even more clones and so on, like a never ending series of Matryoshka dolls. On top of that, some of those Parvatrema doing unlimited fluke works are also able to produce cercariae - the free-swimming larval stages - which then go off to infect more sea snails to start the asexual cycle again. 

So why did they evolve this unique developmental stage? Parvatrema are tiny flukes, the adult stage only live for a few days in the gut of a bird, and they produce less than a hundred eggs - a relatively low number compared with other flukes which may produce thousands or even millions of eggs over their lifetime. To make things worse, the likelihood of any one fluke successfully infecting the right hosts at each consecutive stages of its life cycle is astronomically low, so they need to multiply their numbers at every chance they get.

Furthermore, the final hosts for these flukes are migratory birds which only come once a year - so they need to make the most of their brief stay by making sure that if they only eat one infected snail, instead of just getting a single or a dozen flukes in each snail, they're getting the whole gaggle of fluke clones arriving en masse into the bird's gut in their hundreds or thousands, ready to get on with the business of producing the next generation.

Essentially, these Parvatrema flukes recapitulate the process that most other digenean flukes only undergo in the first host. Asexual reproduction in the first host is arguably one of the key evolutionary innovation of digenean flukes, allowing them to offset the losses associated with the process of being transmitted from one host to the next. Since Parvatrema seems to do asexual reproduction at every possible opportunity, they can provide us with insights into how flukes evolved their one weird asexual trick that gave them an edge in the transmission game.

Reference:

Galaktionov, K. V., Gonchar, A., Postanogova, D., Miroliubov, A., & Bodrov, S. Y. (2024). Parvatrema spp.(Digenea, Gymnophallidae) with parthenogenetic metacercariae: diversity, distribution and host specificity in the Palaearctic. International Journal for Parasitology. 54: 333-355