In interaction with their host organisms, many parasite taxa show an extraordinary degree of specificity, which is often regarded as indication of a long co-evolutionary history. In fact, parasites with a rather narrow range of suitable host species have been shown to be better adapted to sympatric host populations than generalist parasites [1, 2]. However, the actual advantage of being restricted to only one or very few host species is still elusive. Particularly for parasites with complex life cycles, a narrow host range can be very disadvantageous since it decreases the probability for transmission when suitable host species are rare. Therefore, a good strategy for a parasite would be to become optimally adapted to one host species, but capable of a host-switch to avoid extinction when under changing ecological conditions the specific host disappears.
One possibility for a rather fast expansion of the host range could be the introgression of host compatibility genes by hybridization between closely related parasites species . Furthermore, this might also be a way to escape extinction, since specialization has been suggested as a one-way street [4, 5]. Such a scenario is particularly conceivable in macroparasites with complex life cycles, where two parental species are highly specific to different intermediate hosts, but share a common final host where sexual reproduction takes place.
In all major taxa of helminth parasites, hybridization has been found in nature or been demonstrated between sympatric species in laboratory experiments. Most examples have been described in digeneans [6–14], but there is also evidence from cestodes , monogeneans [16, 17] and nematodes [18, 19]. Testing whether or not hybridization may increase fitness by extending the range of suitable (intermediate) host species requires experimental studies to determine transmission success in the different stages of a parasite life cycle. Particularly in schistosomes, several studies have shown that hybrids between two species or strains inherited the ability to develop in both specific host snails of the respective parental lines and retain this increased host range over several generations [14, 20, 21]. Also for behavioral traits related to transmission, like diurnal cercarial shedding patterns  and specificity in host-finding behavior , hybrids of different Schistosoma mansoni strains have been shown to have trait values intermediate between the parental strains,.
Schistocephalus solidus, a cestode with a complex life cycle, is extremely specific for its second intermediate host, infecting only the three-spined stickleback Gasterosteus aculeatus. This system has become a model system for experimental studies on the evolutionary ecology of host-parasite interactions (reviewed by e.g. [24, 25]). Schistocephalus pungitii is closely related to S. solidus, but uses the nine-spined stickleback Pungitius pungitius as second intermediate host, and shows the same host specificity at this level . Both parasites potentially share the same final hosts  and often occur in sympatry [27, 28]. Hence, natural encounters between adults of the sister species are plausible, making hybridization a possibility. However, a recent study by Nishimura and colleagues  shows a deep lineage divergence in the Schistocephalus genus, suggesting that separation of both species occurred shortly after the speciation of their respective stickleback lineages circa 20–25 million years ago. Hybrids have not been observed in nature yet and earlier experiments have shown that both Schistocephalus species are not able to infect the reciprocal intermediate hosts. Additionally, plerocercoids transplanted between three- and nine-spined sticklebacks stopped developing and later on showed destruction of the tegument [30, 31]. Thus, these two species exhibit a high immunological specificity for their second intermediate host.
Many parasites undergo extensive growth in their final host, relative to that in their intermediate hosts . However, Schistocephalus undergoes enormous growth in its second intermediate host. The worm is extensively challenged by the host’s immune system [33, 34], so it is possible that this rapid growth is facilitated by highly specific adaptations to the host’s immune system. At least in vitro, the size of the worm is proportional to egg output [35, 36], suggesting that specificity, growth, and fitness may be tightly linked in this system.
This system offers a unique possibility to investigate host specificity in two closely related parasite species with complex life cycles. It is likely that both parasite species meet in a bird’s gut for reproduction, which could facilitate interspecies mating. Both parasites are simultaneous hermaphrodites and capable of self-fertilization (selfing). Since selfing is costly for the parasite in all stages of its life cycle [37–40], hybridization would seem to be a good way to avoid the negative effects of inbreeding when outcrossing is not possible.
The aim of this study was to investigate the possibility of hybridization between the two cestode species of sticklebacks and the consequences of hybridization for host specificity and fitness at all stages of the parasite’s life cycle.