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 ofCichlidogyrusprobably 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.

We discuss geographical distribution and phylogeny of Dactylogyridea (Monogenea) parasitizing Cichlidae to elucidate their hosts' history. Although mesoparasitic Monogenea (Enterogyrusspp.) show typical vicariant distribution, ectoparasitic representatives from different continents are not considered sister taxa, hence their distribution cannot result from vicariance alone. Because of the close host-parasite relationship, this might indicate that present-day cichlid distribution may also reflect dispersal through coastal or brackish waters. Loss of ectoparasites during transoceanic migration, followed by lateral transfer from other fish families might explain extant host-parasite associations. Because of its mesoparasitic nature, hence not subject to salinity variations of the host's environment,Enterogyruscould have survived marine migrations, intolerable for ectoparasites. Host-switches and salinity transitions may be invoked to explain the pattern revealed by a preliminary morphological phylogeny of monogenean genera from Cichlidae and other selected Monogenea genera, rendering the parasite distribution explicable under both vicariance and dispersal. Testable hypotheses are put forward in this parasitological approach to cichlid biogeography. Along with more comprehensive in-depth morphological phylogeny, comparison with molecular data, clarifying dactylogyridean evolution on different continents and from various fish families, and providing temporal information on host-parasite history, are needed to discriminate between the possible scenarios.

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.

Pariselle A. & Euzet L. 2009. — Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema 31 (4): 849-898. ABSTRACT Systematic revision is made of the six dactylogyridean genera (Monogenea) described on African, Levantine and Malagasy cichlid fishes: Urogyrus Bilong Bilong, Birgi & Euzet, 1994 (including one species); Enterogyrus Paperna, 1963 (including eight species); Insulacleidus Rakotofiringa & Euzet, 1983 (including three species); Onchobdella Paperna, 1968 (including eight species); Scutogyrus Pariselle & Euzet, 1995 (including six species) and Cichlidogyrus Paperna, 1960 (including 71 species). Validities of species are discussed. Diagnoses and illustrated determination keys are given for all taxa. RÉSUMÉ Révision systématique des Monogènes Dactylogyridea parasites de poissons Cichlidae en Afrique, au Proche-Orient et à Madagascar. Les auteurs font la révision systématique des six genres de Monogènes Dactylogyridea connus pour être parasites des poissons Cichlidae en Afrique, au Proche-Orient et à Madagascar: Urogyrus Bilong Bilong, Birgi & Euzet, 1994 (comprenant une espèce) ; Enterogyrus Paperna, 1963 (comprenant huit espèces); Insulacleidus Rakotofiringa & Euzet, 1983 (comprenant trois espèces) ; Onchobdella Paperna, 1968 (comprenant huit espèces); Scutogyrus Pariselle & Euzet, 1995 (comprenant six espèces) et Cichlidogyrus Paperna, 1960 (comprenant 71 espèces). La validité de toutes les espèces est discutée. Les diagnoses et des clés d'identification illustrées sont données pour tous les taxons.

Parasite 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. The 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. Cichlidogyrus 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.. Our 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.