Gyrodactylus crysoleucas, Mizelle and Kritsky, 1967

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 : 8-9

Gyrodactylus crysoleucas : a successfully introduced parasite in the western USA

Considering the morphometric data provided by Mizelle and Kritsky [ 65] when describing G. crysoleucas from non-native N. crysoleucas , intraspecific variability was found in which specimens collected herein from the southcentral location exhibited shorter haptoral parts, mainly the hamuli and ventral bar. Genetically, while published and newly obtained sequences of the 18S rDNA regions of G. crysoleucas were conserved, sequences of the ITS regions demonstrated weak intraspecific variability on the geographical scale. Although genetic data on G. crysoleucas in western freshwaters are missing, the morphological variability between our specimens and the types could be explained by phenotypic plasticity and/or local adaptation in the newly invaded host (habitat) or possibly allopatric isolation. In the Nearctic region, variability in haptoral morphology across distant localities was already documented in G. atratuli Putz and Hoffman, 1963 , a species parasitizing a wide range of leuciscid fish hosts [ 35, 49, 79, 82]. nBLAST search recovered G. crysoleucas and G. salmonis from non-native salmonids with highly conservative 18S rDNA sequences, which is in accordance with the morphotype of their haptoral parts, marked by poorly developed lateral processes of the ventral bar, a short posteriorly-tapering membrane, and marginal hooks with a downward heel and finger-like toe with a prominent shelf [ 92]. Conservative 18S rDNA sequences were reported in the recently described G. hanseni Rahmouni, Seifertová and Šimková, 2023 parasitizing both the striped shiner Luxilus chrysocephalus Rafinesque, 1820 , and the creek chub, Semotilus atromaculatus (Mitchill, 1818) , and in other Gyrodactylus species from native leuciscids and cultured salmonids [ 33, 82].

The present study adds two shiner species to the known hosts of G. crysoleucas across the USA; N. crysoleucas from California [ 65] and Minnesota [ 55], and C. venusta studied herein from Texas. This study presents, thus, new host and locality records for G. crysoleucas . To understand the geographical range of distribution of G. crysoleucas , it is necessary to track the historical origin of N. crysoleucas and C. venusta in the collected areas. According to the USGS database [ 71], both N. crysoleucas and C. venusta are naturally present in Texas and Minnesota, but not in the western part of the USA, including California. In contrast, N. crysoleucas was previously (late 1890s) distributed to multiple water bodies in California as a major bait and forage fish species by the California Fish Commission [ 26] and, since then, it has quickly spread in the western USA [ 98]. This is similar to the red shiner Cyprinella lutrensis (Baird and Girard, 1853) , native to central North America west of the Mississippi River drainage [ 30, 74], which was successfully introduced into California’ s inland waters [ 67]. According to Moyle [ 67], the golden shiner, N. crysoleucas , was introduced to California from more eastern watersheds, which makes G. crysoleucas first described by Mizelle and Kritsky [ 65] from N. crysoleucas sampled in California an alien parasite in the western part of the USA, co-introduced with golden shiner hosts. This scenario is supported by the fact that G. crysoleucas was found herein on wild C. venusta native to Texas and previously on cultured golden shiners in the far North in Minnesota [ 55], where they are often harvested from wild sources, which makes the possibility that G. crysoleucas is of western origin less likely. Nevertheless, this statement requires further investigation since the native parasite fauna in freshwater fish is still underexplored in this region. From native C. lutrensis in Midwestern USA (Nebraska), a single species, G. callawayensis Mayes, 1977 , was described [ 62]. This was interestingly reminiscent of G. crysoleucas regarding the morphotype of the ventral bar characterized by poorly developed lateral processes and a short, posteriorly tapering membrane. The twisted anterior part (tips) to the hamuli is present in G. callawayensis [ 62] but not in G. crysoleucas which discriminates these two species. Since C. lutrensis is non-native in western inland waters, it would be worthwhile to investigate whether the red shiner has co-introduced its native gyrodactylids to Californian freshwaters.

Only a single parasite species, namely, G. baeacanthus , was formally described from C. venusta [ 103], whereas Rahmouni et al. [ 82] recently reported the presence of an undescribed species, Gyrodactylus sp. “ C. venusta ”, highly reminiscent of G. mediotorus isolated herein from C. venusta but also from N. cf. stramineus ( Guadalupe River) (see below). In contrast, two species were recognized on N. crysoleucas additionally to G. crysoleucas [ 55, 65]; they are G. rachelae Price and McMahon, 1967 from the southeast (Tennessee) [ 76], and G. variabilis Mizelle and Kritsky, 1967 from western [ 65], northeast, and southcentral USA, as well as from northeast Canada [ 82]. Interestingly, previous [ 103] and current records of gyrodactylids from C. venusta were made from southern populations occurring in Georgia, Alabama, and Louisiana watersheds and in Texas, all representing the native distributional range of C. venusta [ 30, 70, 74]. In this study, morphological and genetic characterizations indicated that C. venusta hosted G. crysoleucas rather than G. baeacanthus . Two hypotheses may explain this pattern. The first one is that southcentral C. venusta is a native host of G. crysoleucas , making further widescale parasitological investigations of shiner hosts necessary to identify the gyrodactylid fauna in Texas. The second hypothesis is that G. crysoleucas is native to N. crysoleucas and infected a non-congeneric host, C. venusta in this case, by host-switching in overlapped habitats. Host-switching scenarios are common in Gyrodactylus as one major mechanism of speciation [ 72, 111] and have been documented in Nearctic freshwaters [ 82]. Further sampling of N. crysoleucas for the investigation of Gyrodactylus in Texas as well as across the whole range of its current distribution would provide more support for this hypothesis. Further, the natural host-switching of Gyrodactylus is known to be favorable under conditions of high parasite abundance and population growth [ 66] or continuous transmission ability [ 4]. More specific information on the infection rates of G. crysoleucas and on the population density of C. venusta would provide support for the host-switching scenario in southcentral USA.