Gyrodactylus mediotorus, King, Marcogliese, Forest, McLaughlin and Bentzen, 2013

Rahmouni, Chahrazed, Seifertová, Mária, Bean, Megan G. & Šimková, Andrea, 2024, Intraspecific variation in Gyrodactylus mediotorus and G. crysoleucas (Gyrodactylidae) from Nearctic shiners (Leuciscidae): evidence for ongoing speciation, host-switching, and parasite translocation, Parasite (Paris, France) 31 (29), pp. 1-14 : 10-11

Gyrodactylus mediotorus illustrating ongoing speciation in the Nearctic

In the present study, G. mediotorus was isolated from the blacktail and sand shiners, C. venusta and N. cf. stramineus ( Guadalupe River), respectively, both collected in their natural distribution range in Texas. Gyrodactylus mediotorus was originally described on the spottail shiner, N. hudsonius in Canada [ 48], and recently identified from the weed shiner, N. texanus , from the Upper Mississippi River in Wisconsin [ 56]. Therefore, this study presents two new shiner hosts for G. mediotorus and a new locality in the southeast USA. No morphological intraspecific variability of the haptoral hard parts was found in G. mediotorus across the studied shiner hosts. Inversely, the sclerotized structures of G. mediotorus collected from Texas in this study were shorter compared to those in the type-material [ 48]. Moreover, G. mediotorus appeared to possess typical features previously overlooked – specifically, the knob in the median part of the ventral bar and the prominent filament attachment posterior to the handle of marginal hooks. The filament of the marginal hooks is already known to be present in G. spathulatus Mueller, 1936 restricted to catostomid hosts so far [ 20 – 24, 37, 54, 68, 77, 82, 102], and in the generalist G. stunkardi Kritsky and Mizelle, 1968 infecting a range of Nearctic cypriniforms [ 21, 22, 51, 52, 68, 82, 102]. It was also reported in the new but unidentified Gyrodactylus spp. from the blacknose dace, Rhinichthis atratulus , and C. venusta [ 82]. Although morphologically similar to each other and occurring in the southcentral part of the USA, the G. mediotorus we studied herein and Gyrodactylus sp. “ C. venusta ” collected previously in Mississippi most likely belong to two distinct species due to the considerable size variation in the ventral bar [ 82]. DNA sequences of the ITS regions will certainly clarify the taxonomic status of Gyrodactylus sp. “ C. venusta ” in the future. Furthermore, our specimens and those of G. mediotorus from N. texanus [ 56] presented intraspecific variability. This morphological discrepancy can be related to a specific host and/or geographical locality or phenotypic plasticity as previously evidenced in Gyrodactylus communities [ 19, 72, 82]. Sequences of the 18S rDNA and ITS regions of G. mediotorus were successfully obtained in this study and were fully conserved at the host species level. This could be linked to the common evolutionary history of shiners in the Nearctic region [ 96]. On the one hand, in terms of host specificity and similar to remarks by Šimková et al. [ 95], G. mediotorus appears to be an intermediate specialist parasitizing congeneric as well as phylogenetically closely related non-congeneric shiner hosts across the Nearctic region. Alternatively, the presence of G. mediotorus on southcentral populations of C. venusta and N. cf. stramineus ( Guadalupe River) could simply be an inheritance from a common ancestor or has resulted from host-switching. The former scenario seems plausible given the evolutionary relatedness between these shiners [ 96]. The overall Notropis host range associated with G. mediotorus and its phylogenetically closely related G. ticuchi and G. tobala may indicate that host-switching occurred from Notropis spp. to C. venusta rather than the opposite pattern (from C. venusta to Notropis spp. ). Host-switching of Gyrodactylus also seems possible given the close phylogenetic relationship between C. venusta and N. cf. stramineus ( Guadalupe River) and their occurrence in overlapping ecological niches in Texas. In monogeneans of the genus Lamellodiscus ( Diplectanidae ) parasitizing sympatric marine sparid fish hosts, for instance, host-parasite associations have been shown to be mostly driven by ecological factors that considerably facilitated host-switching processes [ 25].

In accordance with the morphological variability observed among all currently available G. mediotorus , i.e., specimens from Canadian N. hudsonius (type-material), from N. texanus of the Upper Mississippi River in Wisconsin, and from both C. venusta and N. cf. stramineus ( Guadalupe River) from Texas, genetic divergence was found, with G. mediotorus from Wisconsin and Texas (both USA) being genetically closer to each other than to the Canadian variant. Values of p- distances (0.9%) even approached the upper limit value (1%) of intraspecific genetic variation in the ITS regions usually considered to discriminate among Gyrodactylus spp. [ 41, 112]. Rahmouni et al. [ 82] questioned the cryptic status of G. huyseae found to parasitize two historically-connected hosts, L. chrysocephalus and N. hudsonius , occurring in overlapping ranges, when the genetic variation in the ITS sequences slightly exceeded the limit value and a single mutation was found in the 18S rDNA sequences. The morphological and genetic divergence of G. mediotorus on the geographical scale evidenced in this study may be explained by the evolutionary history of shiners – particularly, their evolution during the Pleistocene glaciations, which considerably shaped the current distribution of freshwater biotas in North America [ 28, 38]. Hydrographic barriers favoring separate evolutionary pathways in Nearctic freshwaters could also have been involved in creating the morphological and genetic patterns observed in G. mediotorus populations. Ongoing speciation in G. mediotorus is, thus, most likely given the complex combinations of dispersal and vicariance events that shiner hosts have experienced. The geological, climatic, and biotic factors and circumstances that have promoted such speciation remain unknown, but deeper investigations involving powerful genetic approaches using various markers, ideally both nuclear and mitochondrial, will certainly help illuminate how gyrodactylid communities are evolving and adapting to distinct Nearctic fish hosts.

Acknowledgements

The authors are very grateful to all colleagues from the Texas Parks and Wildlife Department, Inland Fisheries, Texas, United States of America for fish collection and identification, and to Eva Řehulková from Masaryk University, Brno, Czech Republic for parasite collection. Special thanks go to Roman Kuchta and Blanka Škoríková (Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic) for kind help with fish dissection, parasite isolation, and fixation, and for assistance with the deposition of voucher specimens at IPCAS, and to Susana Schonhuth from Saint Louis University, USA and Kevin W. Conway from Texas A & M University, USA for their feedback regarding the shiner fish species. We further thank the three anonymous reviewers for their constructive comments.

Funding

This study was funded by the Ministry of Education, Youth and Sports of the Czech Republic, project no. LUAUS 23080. Fish sampling and processing was funded by US Fish and Wildlife Service’ s Sport Fish Restoration Grant to Texas Parks and Wildlife Department. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of Interest

The authors declare that they have no competing interests.

Author contribution statement

AŠ designed and supervised this study and collected parasite specimens. MB co-organized the fish sampling and identified the shiner hosts. CR performed the microscopic observations, identified the parasite species, drew the hard parts, and prepared the species descriptions. MS and CR performed genetic analyses. CR wrote the paper. AŠ, CR, MS, and MB discussed the results. AŠ, MS, and MB revised the manuscript. AŠ acquired funding resources for this study. MB supported the fish sampling and processing. All authors read and approved the final manuscript.