Speciation by Host Switch and Adaptive Radiation in a Fish Parasite Genus Gyrodactylus (Monogenea, Gyrodactylidae)

Abstract

Abstract. Four hundred Gyrodactylus species have been formally described, but the estimated number of species in this fish ectoparasite genus of Monogenean Platyhelminthes is more than 20,000. The unusually high species richness has lead to the hypotheses of speciation and adaptive radiation via host switching. These hypotheses were tested by reconstructing a molecular phylogeny for the subgenus G. (Limnonephrotus) which is a group of freshwater parasites, including five species infecting wild and farmed salmonids. The highly variable ITS1 and ITS2 segments and the conservative 5.8S ribosomal gene were sequenced in 22 species plus two species representing the subgenus G. (Paranephrotus) as an outgroup. The phylogeny was compared with host systematics: the species were collected from six fish families (Cyprinidae, Salmonidae, Percidae, Esocidae, Gasterosteidae, and Gobitidae). The phylogenetic analysis demonstrated that G. (Limnonephrotus) is a monophyletic group that was originally hosted by cyprinids. The speciation has occurred in two episodes, the older one manifested in genetic distances 25-33% (4-6 Myr BP). The latter speciation burst occurred in one clade only, perhaps one million years ago. This clade has been morphologically identified as a wageneri species group. It is a monophyletic group of 18 species [studied here] and contains all five salmonid parasites, but also parasites, on cyprinids, percids, esocids, and gasterosteids. In G. (Limnonephrotus), eight host switches crossing the host family barrier were observed, and at least three of them were followed by repetitive speciation. Seven host-switch events were statistically confirmed by bootstrapping. The suggested model of speciation by host switch was accepted, and interestingly the adaptive radiation seems to be a consequence of host switch to a new family (key innovation model). The molecular and ecological evolution rate of Gyrodactylus parasites is manyfold in comparison to host species, and the phylogenies are largely independent and disconnected.

Biogeographic Hierarchical Levels and Parasite Speciation

“…Such a pattern has previously been noted in the monogeneans (Zietara & Lumme, 2002). This indicates that there is little coevolutionary pattern at the species level, and speciation takes place at the parasite-species/host-family level, coupled with longdistance postdispersal speciation.…”

“…This helps explain why not every freshwater fish has a Rhabdochona species, and why there are only 8000 species of Digenea, while there are more than 40, 000 species of potential vertebrate hosts to be infected (Hugot et al, 2001). A similar observation was inferred from gyrodactylid phylogenies (Simková et al, 2006;Zietara, & Lumme, 2002).…”

Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses

“…For example, Whittall & Hodges [47] found that changes to nectar spur length among different Aquilegia plant species were associated with shifts in specialist pollinators. Host switching is also thought to drive diversification among the estimated 20 000 species of Gyrodactylus fish ectoparasites [48].…”

Co-Speciation of the Ectoparasite Gyrodactylus teuchis (Monogenea, Platyhelminthes) and Its Salmonid Hosts

“…teuchis is very close to the estimate of 5.5% suggested for the ITS region of the nuclear rDNA cluster of Gyrodactylus , an estimate derived from vicariance of G . aphyae on the Eurasian minnow ( Phoxinus phoxinus ) on opposite sides of the Baltic–White Sea watershed [15]. This seems surprising as mitochondrial DNA in animals generally evolves substantially faster than nuclear loci, but the variation among taxonomic groups is large, and for some basal groups (e.g.…”

“…Additionally, species of Gyrodactylus are capable of both sexual and asexual reproduction and new parasite populations may frequently originate from single founder individuals [14]. Given these unique reproductive features it is not surprising that host switching is believed to be the most abundant mode of speciation in Gyrodactylus [15]. Paradoxically, many Gyrodactylus species are highly host specific [12,16], a trait which is considered to result from the continuous adaptation inherent in a co-evolutionary arms race as first envisioned by Darwin [17].…”