Digeneans are parasitic flatworms with complex life cycles involving two stages of reproduction—sexual and parthenogenetic (asexual). Parthenogenetic reproduction in the first intermediate hosts (FIH, almost exclusively molluscs) has contributed significantly to the thriving of this taxon (Cribb et al., 2003, Galaktionov and Dobrovolskij, 2003, Galaktionov, 2016). Despite this evolutionary role, we still do not quite know how the complex life cycle originated and how the molluscan FIH was adopted, largely due to the lack of paleontological data (Littlewood and Donovan, 2003). Modern models could give some clue to these historical processes, and good candidates are members of the family Gymnophallidae featuring a unique phenomenon — parthenogenetic reproduction of metacercariae (PM) in the second intermediate host (SIH) (Szidat, 1962, James, 1964, Ching, 1982, Irwin et al., 2003). Metacercaria, and cercaria, are generally accepted to be the evolutionarily youngest phases of the digenean life cycle (Ginetsinskaya, 1968, Pearson, 1972, Gibson, 1987, Cribb et al., 2003, Galaktionov and Dobrovolskij, 2003). Therefore, the study of the interrelationships between the gymnophallid PM and their SIH may shed light on the initial stages of colonisation of FIH by digeneans.

In the basic gymnophallid life cycle, bivalves serve as FIH and contain cercariae-producing sporocysts (Bartoli, 1972, Bartoli, 1981; Scholz, 2002; Cremonte et al., 2015). Cercariae are released into the external environment and in most species infect other bivalves (SIH), where non-encysted metacercariae (M) develop. They infect the definitive hosts (DH), coastal birds, following trophic transmission. Gymnophallus australis Szidat, 1962 is the only species with PM developing in bivalves (Szidat, 1962, Cremonte et al., 2008). In the genus Parvatrema, there are species with PM developing in gastropods (James, 1964, Ching, 1982, Galaktionov et al., 2006).

Following penetration into the SIH, undifferentiated cells start proliferating intensely in the genital primordium of the larva. They disperse over the whole metacercarial body and give rise to numerous germinal cells, which start cleavage (Irwin et al., 2003). Also, a digestive system with a bifurcated gut develops, and the number of flame cells in the excretory system increases compared with the cercariae (James, 1964, Galaktionov et al., 2006). These primary PM (PM1) feed intensely, grow and produce the second-generation PM (PM2). They rupture the PM1 body wall and continue independent existence in the molluscan host. The structure of PM2 is virtually the same as that of PM1.

Two variants of the life cycles of the Parvatrema spp. with PM have been described. The type I life cycle is found in Parvatrema homoeotecnum James, 1964 and Parvatrema margaritense (Ching, 1982) Galaktionov, Irwin & Saville, 2006: two generations of PM (PM1 and PM2) develop sequentially in the SIH (James, 1964, Ching, 1982, Podlipajev, 1979, Galaktionov, 1996, Irwin et al., 2003, Galaktionov et al., 2006) (Fig. 1A). In PM2, the third-generation M are formed; they look like typical gymnophallid metacercariae and are invasive for the DH. Fully-formed M stay inside PM2 and so do not directly parasitize the SIH.

The type II life cycle is found in Cercaria falsicingulae I Galaktionov, 2007: PM develop in the SIH and produce furcated cercariae characteristic of gymnophallids (Galaktionov, 2007) (Fig. 1B). The fate of these cercariae varies. Some of them turn into the PM of the next generation within the same host, and further produce either cercariae and PM, or M invasive for the DH. Other cercariae leave the host and infect new molluscs of the same species, where PM form and all the same stages of the cycle as in the primary SIH are repeated. Presumably, the PM–cercariae–PM part of the cycle can go on indefinitely (at least during the warm season) and thus has a certain autonomy (Galaktionov, 2007). Invasive M stay inside the PM.

During our studies in the northern European seas and in the Sea of Okhotsk, Parvatrema spp. with PM were found in several coastal gastropods. The analysis of molecular markers, morphology, and biology of these larvae allowed us to differentiate a complex of five closely related species, to hypothesise how they colonised their gastropod SIH, and to suggest the nature of their geographical expansion. We also discuss these results in the context of early digenean evolution.