Intraspecific variation in Gyrodactylus mediotorus and G. crysoleucas (Gyrodactylidae) from Nearctic shiners (Leuciscidae): evidence for ongoing speciation, host-switching, and parasite translocation.

A parasitological investigation of Cyprinella venusta and Notropis cf. stramineus sampled in Texas, USA, in the Guadalupe River, revealed the presence of Gyrodactylus crysoleucas Mizelle and Kritsky, 1967 on C. venusta, and Gyrodactylus mediotorus King, Marcogliese, Forest, McLaughlin & Bentzen, 2013 on both fish species. This represents new leuscicid fish hosts and locality records for these two gyrodactylids. Gyrodactylus crysoleucas previously identified from both non-native Californian Notemigonus crysoleucas and from farmed stocks in Minnesota demonstrated intraspecific variability in terms of morphology and genetics as a local adaptation associated with isolation by distance. Results further confirmed G. crysoleucas as alien in the western USA and suggested host-switching involving C. venusta and N. crysoleucas. Conservative morphology and genetics on the part of G. mediotorus from C. venusta and N. cf. stramineus (Guadalupe River) was observed, while higher genetic divergence in the ITS sequences associated with morphological discrepancy was found between the studied G. mediotorus specimens and those of Notropis hudsonius than when considering the parasites of Notropis texanus. The separation of G. mediotorus into geographical subgroups may indicate ongoing speciation linked to the Pleistocene glaciations in North America, and to hydrographic barriers that facilitated separate evolutionary paths leading to speciation. We suggest that deep investigations of Gyrodactylus populations will help to understand the speciation of these parasites and their adaptation to Nearctic fish hosts.

Title: Variation intraspécifique chez Gyrodactylus mediotorus et G. crysoleucas (Gyrodactylidae), parasites de ménés néarctiques (Leuciscidae) : preuves d'une spéciation en cours, d'un changement d'hôte et d'une translocation de parasites. Abstract: Une enquête parasitologique sur Cyprinella venusta et Notropis cf. stramineus échantillonnés au Texas, États-Unis, dans la rivière Guadalupe, a révélé la présence de Gyrodactylus crysoleucas Mizelle et Kritsky, 1967 sur C. venusta, et de Gyrodactylus mediotorus King, Marcogliese, Forest, McLaughlin & Bentzen, 2013 sur les deux espèces de poissons. Ceci représente de nouveaux poissons Leuciscidae hôtes et des nouvelles localités pour ces deux Gyrodactylidae. Gyrodactylus crysoleucas, identifié précédemment à partir de Notemigonus crysoleucas californiens non indigènes et de stocks d'élevage du Minnesota a démontré une variabilité intraspécifique en termes de morphologie et de génétique en tant qu'adaptation locale associée à l'isolement par la distance. Les résultats ont en outre confirmé que G. crysoleucas était exotique dans l'ouest des États-Unis et ont suggéré un changement d'hôte impliquant C. venusta et N. crysoleucas. Une morphologie et une génétique conservatrices pour G. mediotorus de C. venusta et N. cf. stramineus (rivière Guadalupe) ont été observées, tandis qu'une divergence génétique plus élevée dans les séquences ITS, associée à une divergence morphologique, a été trouvée chez les spécimens étudiés de G. mediotorus et de Notropis hudsonius lorsque l'on considère les parasites de Notropis texanus. La séparation de G. mediotorus en sous-groupes géographiques peut indiquer une spéciation continue liée aux glaciations du Pléistocène en Amérique du Nord et à des barrières hydrographiques qui ont facilité des chemins évolutifs séparés menant à la spéciation. Nous suggérons que des études approfondies sur les populations de Gyrodactylus aideront à comprendre la spéciation de ces parasites et leur adaptation aux poissons hôtes néarctiques.

Revealing the hidden diversity of Gyrodactylus communities (Monogenea, Gyrodactylidae) from Nearctic Catostomidae and Leuciscidae fish hosts (Teleostei, Cypriniformes), with descriptions of ten new species.

Despite the high diversity of freshwater fishes in the Nearctic region, little is known about the composition of their parasite communities. We addressed the diversity of viviparous monogeneans of Gyrodactylus parasitizing highly diversified cypriniform fish inhabiting Nearctic watersheds. Nowadays, a thorough assessment of Gyrodactylus spp. diversity requires both morphological traits and genetic data. A combination of taxonomically important haptoral features and sequences of the ITS regions and 18S rDNA revealed 25 Gyrodactylus spp. parasitizing two catostomid and 15 leuciscid species sampled in six distinct localities in the United States and Canada. These include ten Gyrodactylus species recognized as new to science and described herein (G. ellae n. sp., G. hamdii n. sp., G. hanseni n. sp., G. huyseae n. sp., G. kuchtai n. sp., G. lummei n. sp., G. mendeli n. sp., G. prikrylovae n. sp., G. scholzi n. sp., and G. steineri n. sp.), seven already known species, and finally eight undescribed species. Overall, Nearctic Gyrodactylus spp. exhibited haptoral morphotypes known from fish hosts worldwide and those apparently restricted to Nearctic Gyrodactylus lineages like the typical ventral bar with a median knob and a plate-like membrane, or the additional filament attached to the handles of marginal hooks. The integrative approach further evidenced possible ongoing gene flow, host-switching in generalist Gyrodactylus spp., and regional translocation of monogenean fauna through fish introductions. The study highlights the hitherto underexplored morphological and genetic diversity of viviparous monogeneans throughout the Nearctic region.

Title: Révélation de la diversité cachée des communautés de Gyrodactylus (Monogenea, Gyrodactylidae) des poissons hôtes néarctiques Catostomidae et Leuciscidae (Teleostei, Cypriniformes), avec la description de dix nouvelles espèces. Abstract: Malgré la grande diversité des poissons d'eau douce dans la région néarctique, on sait peu de choses sur la composition de leurs communautés de parasites. Nous avons abordé la diversité des monogènes vivipares du genre Gyrodactylus parasitant des poissons cypriniformes très diversifiés habitant les bassins versants néarctiques. De nos jours, une évaluation approfondie de la diversité de Gyrodactylus spp. nécessite à la fois des traits morphologiques et des données génétiques. Une combinaison de caractéristiques haptorales et de séquences taxonomiquement importantes des régions ITS et de l'ADNr 18S a révélé 25 espèces de Gyrodactylus sur deux espèces de catostomidés et 15 espèces de leuciscidés échantillonnées dans six localités distinctes aux États-Unis et au Canada. Celles-ci comprennent dix espèces de Gyrodactylus reconnues comme nouvelles pour la science et décrites dans cette étude (G. ellae n. sp., G. hamdii n. sp., G. hanseni n. sp., G. huyseae n. sp., G. kuchtai n. sp., G. lummei n. sp., G. mendeli n. sp., G. prikrylovae n. sp., G. scholzi n. sp. et G. steineri n. sp.), sept espèces déjà connues et enfin huit espèces non décrites. Dans l'ensemble, les espèces de Gyrodactylus néarctiques présentaient des morphotypes haptoraux connus chez les poissons hôtes du monde entier et ceux apparemment limités aux lignées néarctiques de Gyrodactylus comme la barre ventrale typique avec un bouton médian et une membrane en forme de plaque, ou le filament supplémentaire attaché aux poignées des crochets marginaux. L'approche intégrative a en outre mis en évidence le flux de gènes en cours, le changement d'hôte chez les espèces de Gyrodactylus généralistes et la translocation régionale de la faune monogène par l'introduction de poissons. L'étude met en évidence la diversité morphologique et génétique jusqu'ici sous-explorée des monogènes vivipares dans toute la région néarctique.

Molecular phylogeny and speciation patterns in host-specific monogeneans (Cichlidogyrus, Dactylogyridae) parasitizing cichlid fishes (Cichliformes, Cichlidae) in Lake Tanganyika.

Cichlidogyrus (including Scutogyrus) is the most speciose dactylogyridean monogenean genus known from African and Levantine cichlid fishes (Cichlidae). While its taxonomy is well established, little is known about the phylogenetic relationships and evolutionary history of this ectoparasite, especially from hosts belonging to one of the most impressive vertebrate radiations, the cichlid fishes from the East African Great Lakes and surrounding hydrological systems. Phylogenetic inference based on DNA sequences of the nuclear 18S, internal transcribed spacer 1 and 28S rDNA genes revealed that Cichlidogyrus parasitizing mainly West African cichlid tribes is paraphyletic with respect to species parasitizing hosts belonging to the East African cichlid radiation, which constitute a well-supported monophylum. Members of Cichlidogyrus from tylochromine and oreochromine hosts that colonised Lake Tanganyika only recently, cluster with their non-Lake Tanganyika relatives, indicating that they colonised Lake Tanganyika with their current host species, and did not jump over from any of the many cichlid species already present in the lake. The diversification of Cichlidogyrus in Lake Tanganyika seems to be driven by failure to diverge in old lineages of cichlids, cospeciation in more recently evolved ones, and host switching followed by parasite duplication at the level of the various host tribes. Evaluation of host specificity and structural evolution of haptoral and reproductive organs in Lake Tanganyika Cichlidogyrus revealed that strict specialist species together with larval hook size represent the ancestral state of haptor configuration, suggesting that members of Cichlidogyrus in this system evolved from a very simple form to a more complex one similarly to their West African congeners. Generalist species among Cichlidogyrus with a sclerotized vagina parasitizing ancient Lake Tanganyika lineages seem to have developed a different hook configuration, most probably to ensure successful colonisation of new, phylogenetically unrelated hosts.

Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika.

Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) isolated from the gills of six cichlid host species belonging to four tribes and sampled from the Congolese coastline of Lake Tanganyika (LT) are described: Cichlidogyrus adkoningsi sp. nov. from Cyphotilapia frontosa (tribe Cyphotilapiini); C. koblmuelleri sp. nov. from Cardiopharynx schoutedeni (Ectodini); C. habluetzeli sp. nov. from C. schoutedeni and C. frontosa; C. antoineparisellei sp. nov. from Interochromis loocki (Tropheini); C. masilyai sp. nov. from Petrochromis orthognathus (Tropheini); C. salzburgeri sp. nov. from P. trewavasae, and C. sergemorandi sp. nov. from Tylochromis polylepis (Tylochromini). This study represents the first parasitological examination of cyphotilapiine cichlid hosts. Representatives of the Tanganyikan ectodine, tropheine, and tylochromine cichlids previously sampled from various localities in the lake yielded nine, twelve, and two described species of Cichlidogyrus, respectively. The study further includes a morphological characterization of the male copulatory organ of six undescribed species of Cichlidogyrus found on the gills of the tropheines I. loocki and P. orthognathus, and on those of Callochromis melanostigma and Xenotilapia flavipinnis (both Ectodini). Geographical variation in the monogenean fauna of I. loocki was observed. The most closely related cichlid species investigated in this study harboured Cichlidogyrus spp. exhibiting some similarities in their sclerotized structures. Thus, our paper provides additional evidence of the high species richness of Cichlidogyrus and the link with their hosts's phylogenetic affinities in LT.

Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ.

BACKGROUND: Lake Tanganyika harbours the most diverse cichlid assemblage of the Great African Lakes. Considering its cichlid flocks consist of approximately 250 endemic species, we can hypothesize a high species-richness in their often quite host-specific monogenean ectoparasites belonging to Cichlidogyrus Paperna, 1960. Yet, only 24 species were described from Tanganyikan hosts and some host tribes have never been investigated for monogeneans. This study presents the first parasitological examination of species of the tribes Cyprichromini (Cyprichromis microlepidotus (Poll, 1956)), Eretmodini (Eretmodus marksmithi Burgess, 2012 and Tanganicodus irsacae Poll, 1950) and Ectodini (Aulonocranus dewindti (Boulenger, 1899)). Specimens of the ectodine Ophthalmotilapia nasuta (Poll & Matthes, 1962) from which four Cichlidogyrus spp. have been previously described from more southern localities were also studied. Further, we discuss the haptor configuration in Tanganyikan Cichlidogyrus spp. and highlight the morphological diversity of the vagina, and that of the heel, a sclerotized part of the male copulatory organ, absent in some species of Cichlidogyrus. METHODS: Cichlidogyrus spp. were isolated from gills and fixed using GAP. Haptoral and genital hard parts were measured and drawn by means of a phase contrast microscopic examination. RESULTS: We describe eight new species: Cichlidogyrus milangelnari n. sp. on C. microlepidotus; C. jeanloujustinei n. sp. on E. marksmithi; C. evikae n. sp. on T. irsacae; C. aspiralis n. sp., C. glacicremoratus n. sp. and C. rectangulus n. sp. on O. nasuta; and C. pseudoaspiralis n. sp. and C. discophonum n. sp. on A. dewindti. Three haptoral morphotypes were recognized among the new species. Species of Cichlidogyrus from closely related hosts exhibited the same morphotypes. Geographical variation in Cichlidogyrus spp. fauna as observed in O. nasuta and three morphotypes were distinguished. Finally, we listed 111 Cichlidogyrus species, of which 27 and three Tanganyikan species lack sclerotized vagina and heel, respectively, just like 19 and seven species outside of the lake. CONCLUSIONS: Haptoral and genital features in the Tanganyikan Cichlidogyrus fauna reflect the phylogenetic relationships of their cichlid hosts. It seems that several lineages of Cichlidogyrus spp. exist in Lake Tanganyika but further studies are necessary to confirm this hypothesis and answer questions related to Lake Tanganyika and its cichlids.

The monogenean which lost its clamps.

Ectoparasites face a daily challenge: to remain attached to their hosts. Polyopisthocotylean monogeneans usually attach to the surface of fish gills using highly specialized structures, the sclerotized clamps. In the original description of the protomicrocotylid species Lethacotyle fijiensis, described 60 years ago, the clamps were considered to be absent but few specimens were available and this observation was later questioned. In addition, genera within the family Protomicrocotylidae have either clamps of the "gastrocotylid" or the "microcotylid" types; this puzzled systematists because these clamp types are characteristic of distinct, major groups. Discovery of another, new, species of the genus Lethacotyle, has allowed us to explore the nature of the attachment structures in protomicrocotylids. Lethacotyle vera n. sp. is described from the gills of the carangid Caranx papuensis off New Caledonia. It is distinguished from Lethacotyle fijiensis, the only other species of the genus, by the length of the male copulatory spines. Sequences of 28S rDNA were used to build a tree, in which Lethacotyle vera grouped with other protomicrocotylids. The identity of the host fish was confirmed with COI barcodes. We observed that protomicrocotylids have specialized structures associated with their attachment organ, such as lateral flaps and transverse striations, which are not known in other monogeneans. We thus hypothesized that the clamps in protomicrocotylids were sequentially lost during evolution, coinciding with the development of other attachment structures. To test the hypothesis, we calculated the surfaces of clamps and body in 120 species of gastrocotylinean monogeneans, based on published descriptions. The ratio of clamp surface: body surface was the lowest in protomicrocotylids. We conclude that clamps in protomicrocotylids are vestigial organs, and that occurrence of "gastrocotylid" and simpler "microcotylid" clamps within the same family are steps in an evolutionary sequence, leading to the absence of these attributes in species of Lethacotyle.