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

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.

The first report of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) on Italian cultured stocks of rainbow trout (Oncorhynchus mykiss Walbaum)

“…The discrimination of G. salaris from other related species is, however, not always straightforward. Gyrodactylus salaris and the purported non-pathogenic Gyrodactylus thymalli Žitň an, 1960 from grayling, Thymallus thymallus L., are morphologically similar, their ITS sequences are practically identical, and recent studies indicate that the two species might be conspecific (Zię tara and Lumme, 2002;Hansen et al, 2003Hansen et al, , 2006Hansen et al, , 2007Meinilä et al, 2004). Analyses of the mitochondrial cytochrome oxidase I gene (COI), however, show that G. salaris and G. thymalli can be grouped in different clades and that all the gyrodactylids from rainbow trout appear to belong to the same COI haplotype (Hansen et al, 2003;Meinilä et al, 2004).…”

“…(Matejusová et al, 2001;Zię tara and Lumme, 2002). The discrimination of G. salaris from other related species is, however, not always straightforward.…”

Ribosomal DNA as molecular markers and their applications in the identification of fish parasites (Platyhelminthes: Monogenea) from India

“…Control and treatment of parasitic infection depends upon proper and quick identification of related parasites. The morphological species perception is based on the observed discontinuities, and it is non-dimensional, without good information about the fine-scale (species level) evolution [11] . Taxonomy underpins all biological research, with implications for many scientific and applied fields but this comes at a time when taxonomy is facing a crisis, because fewer specialists are available.…”

Especiação e seus mecanismos: histórico conceitual e avanços recentes

“…Um exemplo bastante claro desse efeito é observado em Gyrodactylus Nordmann, 1832, Monogenea (Platyhelminthes) que reúne mais de quatrocentas espécies ectoparasitas de peixes (Zietara, Lumme, 2002). Esses autores explicam que a especiação e a radiação adaptativa devidas à mudança de hospedeiro têm sido a hipótese apresentada para justificar a riqueza incomum das espécies do gênero.…”

“…Essa oportunidade de migração também aumenta quando comparada com outras espécies parasitas que só realizam a transmissão uma única vez, durante o estágio larval. Portanto, no percurso da evolução, a mudança para uma nova espécie de hospedeiro deve preceder o evento de especiação e guiar as demais alterações necessárias, como a resistência mecânica, tolerância contra defesas e elevada capacidade de explorar os novos recursos (Kuusela, Zietara, Lumme, 2008;Zietara, Lumme, 2002). Essas características são comumente observadas entre os Gyrodactylidae, tanto em análises empíricas quanto experimentais (Kuusela, Zietara, Lumme, 2008).…”