Distinct Lineages of Schistocephalus Parasites in Threespine and Ninespine Stickleback Hosts Revealed by DNA Sequence Analysis

Abstract

Parasitic interactions are often part of complex networks of interspecific relationships that have evolved in biological communities. Despite many years of work on the evolution of parasitism, the likelihood that sister taxa of parasites can co-evolve with their hosts to specifically infect two related lineages, even when those hosts occur sympatrically, is still unclear. Furthermore, when these specific interactions occur, the molecular and physiological basis of this specificity is still largely unknown. The presence of these specific parasitic relationships can now be tested using molecular markers such as DNA sequence variation. Here we test for specific parasitic relationships in an emerging host-parasite model, the stickleback-Schistocephalus system. Threespine and ninespine stickleback fish are intermediate hosts for Schistocephalus cestode parasites that are phenotypically very similar and have nearly identical life cycles through plankton, stickleback, and avian hosts. We analyzed over 2000 base pairs of COX1 and NADH1 mitochondrial DNA sequences in 48 Schistocephalus individuals collected from threespine and ninespine stickleback hosts from disparate geographic regions distributed across the Northern Hemisphere. Our data strongly support the presence of two distinct clades of Schistocephalus, each of which exclusively infects either threespine or ninespine stickleback. These clades most likely represent different species that diverged soon after the speciation of their stickleback hosts. In addition, genetic structuring exists among Schistocephalus taken from threespine stickleback hosts from Alaska, Oregon and Wales, although it is much less than the divergence between hosts. Our findings emphasize that biological communities may be even more complex than they first appear, and beg the question of what are the ecological, physiological, and genetic factors that maintain the specificity of the Schistocephalus parasites and their stickleback hosts.

The role of prezygotic isolation mechanisms in the divergence of two parasite species

“…Studies on gene flow of different species or populations of Schistocephalus are still rare [35] and should also consider the possibility of gene flow between these two species in the future. According to our results, there is no evidence for an efficient prezygotic reproductive barrier.…”

“…Nishimura et al [35] suggested that speciation occurred shortly after the divergence of the two stickleback species as a single event, which would argue for a co-speciation following the divergence of the stickleback species. The strong separation indicated by molecular data suggests low or no gene flow between these two parasite species, even though extensive studies on this have not yet been conducted.…”

“…Even though the two cestode species successfully interbreed under laboratory conditions, so far there is no evidence for hybridization from natural populations [35]. This is particularly surprising because an expansion of the extremely narrow second intermediate host range is presumably highly advantageous for the parasite’s chance of developing into a plerocercoid infective to the definitive bird host.…”

A Review of Molecular Approaches for Investigating Patterns of Coevolution in Marine Host–Parasite Relationships

“…This marker was chosen (in combination with ITS1) by Criscione and Blouin (2004) to identify cryptic salmon trematode species. A combination of COI mtDNA and NADH1 was used on cestode species within three-spine (G. aculeatus) and nine-spine (Pungitius pungitius) stickleback hosts (Nishimura et al, 2011). Here, the divisional pattern of mtDNA sequences delivered strong evidence for the presence of two cryptic cestode species, where one exclusively infects three-spine sticklebacks and the other one only the nine-spine stickleback.…”

Hybridization between two cestode species and its consequences for intermediate host range

“…Hence, natural encounters between adults of the sister species are plausible, making hybridization a possibility. However, a recent study by Nishimura and colleagues [29] 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.…”