Cichlidogyrus spp. (Monogenea, Ancyrocephalidae) are common parasites of cichlid fishes from Africa and the Levant. They display important morphological variation in their attachment apparatus and infect a broad host spectrum throughout a wide geographic range. Thus, they offer an interesting model to investigate to what extent the phenotypic variability of the attachment organ among congeners is related to host specificity, geographic/ environmental components, or phylogeny. A geometric morphometric approach was carried out to analyse the shape variation of sclerotized structures of the attachment organ within 66 African species of the genus Cichlidogyrus. The interspecific shape comparison supports the presence of three main morphological configurations, each consisting of a given combination of particular sclerite shapes. Moreover, data emphasize strong coordination and integration (shape co-variation) among the different sclerites jointly forming the attachment organ. Although attachment apparatuses are usually considered to be the result of adaptive processes and must be adapted to the hosts and local environmental conditions, we found no relationship between these clusters and host specificity or geographical distribution. Nevertheless, groups are partially congruent with those obtained with the molecular phylogeny of a subset of species, suggesting a phylogenetic constraint rather than an adaptation to either hosts or environment. Because of the necessity to form a functional entity, modularity within attachment organ imposes important evolutionary constraint. This provides new insights into the evolvability of attachment organs, as well as into the morphological basis of host specificity and host-parasite co-evolutionary interaction in helminth parasites.
The goals of this paper were to investigate phylogenetic and evolutionary patterns of cichlid fish from West Africa and their Cichlidogyrus and Scutogyrus monogenean parasites, to uncover the presence of host-parasite cospeciation and to assess the level of morphological adaptation in parasites. This required the following steps, each one representing specific objectives of this paper: (1) to build phylogenetic trees for Cichlidogyrus and Scutogyrus species based on ribosomal DNA sequences, (2) to investigate phylogenetic relationships within West African cichlid fish based on the analysis of mitochondrial cytochrome b DNA sequences, (3) to investigate host-parasite cophylogenetic history to gain clues on parasite speciation process, and (4) to investigate the link between the morphology of the attachment apparatus and parasite phylogeny. Phylogenetic analyses supported the monophyletic origin of the Cichlidogyrus/Scutogyrus group, and suggested that Cichlidogyrus is polyphyletic and that Scutogyrus is monophyletic. The phylogeny of Cichlidae supported the separation of mouthbrooders and substrate-brooders and is consistent with the hypothesis that the mouthbrooding behavior of Oreochromis and Sarotherodon evolved from substrate-brooding behavior. The mapping of morphological characters of the haptor onto the parasite phylogenetic tree suggests that the attachment organ has evolved from a very simple form to a more complex one. The cophylogenetic analyses indicated a significant fit between trees using distance-based tests, but no significant cospeciation signal using tree-based tests, suggesting the presence of parasite duplications and host switches on related host species. This shed some light on the diversification process of Cichlidogyrus species parasitizing West African cichlids.
The stunning diversity of cichlid fishes has greatly enhanced our understanding of speciation and radiation. Little is known about the evolution of cichlid parasites. Parasites are abundant components of biodiversity, whose diversity typically exceeds that of their hosts. In the first comprehensive phylogenetic parasitological analysis of a vertebrate radiation, we study monogenean parasites infecting tropheine cichlids from Lake Tanganyika. Monogeneans are flatworms usually infecting the body surface and gills of fishes. In contrast to many other parasites, they depend only on a single host species to complete their lifecycle. Our spatially comprehensive combined nuclear-mitochondrial DNA dataset of the parasites covering almost all tropheine host species (N = 18), reveals species-rich parasite assemblages and shows consistent host-specificity. Statistical comparisons of host and parasite phylogenies based on distance and topology-based tests demonstrate significant congruence and suggest that host-switching is rare. Molecular rate evaluation indicates that species of Cichlidogyrus probably diverged synchronically with the initial radiation of the tropheines. They further diversified through within-host speciation into an overlooked species radiation. The unique life history and specialisation of certain parasite groups has profound evolutionary consequences. Hence, evolutionary parasitology adds a new dimension to the study of biodiversity hotspots like Lake Tanganyika.
This study represents the first exploration of the parasite fauna of cichlid fishes in the Mweru-Luapula subregion (Central Africa). Twelve species of cichlids and 14 species of Monogenea from three genera (Cichlidogyrus, Gyrodactylus and Scutogyrus) were collected. We present a first record of the gill parasite fauna of eight host species, Oreochromis mweruensis, Orthochromis sp. 'Mambilima', Sargochromis mellandi, Serranochromis angusticeps, S. stappersi, S. thumbergi and Tylochromis mylodon. The host range of ten parasite species was expanded. The study further includes the description of Cichlidogyrus consobrini sp. n. from S. mellandi and Orthochromis sp. 'Mambilima'. A new morphotype of C. halli is characterized, and three species - C. papernastrema, C. quaestio and C. zambezensis - are redescribed. Furthermore, the biodiversity and host specificity of these parasites is compared with that of cichlid parasites from Lake Kariba and Cameroon. Two species, including C. consobrini sp. n. and a new morphotype of C. halli, are putative endemics. The parasite fauna in Bangweulu-Mweru is highly similar in species composition to Lake Kariba, but in Bangweulu-Mweru the same parasite species are more host-specific, probably because of hydrogeographical differences between the two regions.
BackgroundParasite switches to new host species are of fundamental scientific interest and may be considered an important speciation mechanism. For numerous monogenean fish parasites, infecting different hosts is associated with morphological adaptations, in particular of the attachment organ (haptor). However, haptoral morphology in Cichlidogyrus spp. (Monogenea, Dactylogyridea), parasites of African cichlids, has been mainly linked to phylogenetic rather than to host constraints. Here we determined the position of Cichlidogyrus amieti, a parasite of species of Aphyosemion (Cyprinodontiformes, Nothobranchiidae) in the phylogeny of its congeners in order to infer its origin and assess the morphological changes associated with host-switching events.MethodsThe DNA of specimens of C. amieti isolated from Aphyosemion cameronense in Cameroon was sequenced and analyzed together with that of Cichlidogyrus spp. from cichlid hosts. In order to highlight the influence of the lateral transfer of C. amieti on the haptoral sclerotised parts we performed a Principal Component Analysis (PCA) to compare the attachment organ structure of C. amieti to that of congeners infecting cichlids.ResultsCichlidogyrus amieti was found to be nested within a strongly supported clade of species described from Hemichromis spp. (i.e. C. longicirrus and C. dracolemma). This clade is located at a derived position of the tree, suggesting that C. amieti transferred from cichlids to Cyprinodontiformes and not inversely. The morphological similarity between features of their copulatory organs suggested that C. amieti shares a recent ancestor with C. dracolemma. It also indicates that in this case, these organs do not seem subjected to strong divergent selection pressure. On the other hand, there are substantial differences in haptoral morphology between C. amieti and all of its closely related congeners described from Hemichromis spp..ConclusionsOur study provides new evidence supporting the hypothesis of the adaptive nature of haptor morphology. It demonstrates this adaptive component for the first time within Cichlidogyrus, the attachment organs of which were usually considered to be mainly phylogenetically constrained.
Species interactions are a key aspect of evolutionary biology. Parasites, specifically, are drivers of the evolution of species communities, and impact biosecurity and public health. However, when using interaction networks for evolutionary studies, interdependencies between distantly related species in these networks are shaped by ancient and complex processes. We propose using recent interacting host-parasite radiations, e.g. African cichlid fishes and cichlid gill parasites belonging to Cichlidogyrus (Dactylogyridae, Monogenea), as macroevolutionary model of species interactions. The cichlid-Cichlidogyrus network encompasses 138 parasite species and 416 interactions identified through morphological characteristics and genetic markers in 160 publications. We discuss the steps required to develop this model system based on data resolution, sampling bias, and reporting quality. In addition, we propose the following steps to guide efforts for a macroevolutionary model system for species interactions:First, evaluating and expanding model system outcome measures to increase data resolution. Second, closing knowledge gaps to address underreporting and sampling bias arising from limited human and financial resources.Identifying phylogenetic and geographic targets, creating systematic overviews, enhancing scientific collaborations, and avoiding data loss through awareness of predatory journal publications, can accelerate this process. Third, standardising data reporting to increase reporting quality and to facilitate data accessibility.
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