A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus Françoise Messu Mandeng, Charles Bilong Bilong, Antoine Pariselle, Maarten Vanhove, Arnold Bitja Nyom, Jean-François Agnèse To cite this version: Françoise Messu Mandeng, Charles Bilong Bilong, Antoine Pariselle, Maarten Vanhove, Arnold Bitja Nyom, et al.. A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology ofthis parasite genus. Parasites and Vectors, BioMed Central, 2015, 8 (1), 10.1186/s13071-015-1181-y. hal-01923290 HAL Id: hal-01923290 https://hal.archives-ouvertes.fr/hal-01923290 Submitted on 8 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Messu Mandeng et al. Parasites & Vectors (2015) 8:582 DOI 10.1186/s13071-015-1181-y RESEARCH Open Access A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus Françoise D. Messu Mandeng1,7, Charles F. Bilong Bilong1, Antoine Pariselle2,8*, Maarten P. M. Vanhove3,4,5,9, Arnold R. Bitja Nyom6 and Jean-François Agnèse2 Abstract Background: 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. Methods: 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. Results: 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.. (Continued on next page) * Correspondence: [email protected] 2Institut des Sciences de l’Évolution, IRD UMR 226, CNRS UMR 5554, Université de Montpellier, CC 63, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France 8Present address: IRD, BP 1857, Yaoundé, Cameroon Full list of author information is available at the end of the article © 2015 Messu Mandeng et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Messu Mandeng et al. Parasites & Vectors (2015) 8:582 Page 2 of 12 (Continued from previous page) Conclusions: 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. Keywords: Phylogeny, Lateral transfer, Cichlidogyrus amieti, Aphyosemion, Nothobranchiidae, Cichlidae, Cameroon, Africa Background congeners infecting non‐cichlids such as Cichlidogyrus Teleost fishes of the order Cyprinodontiformes, com- amieti have not yet been included in these analyses. monly called cyprinodonts, or rivulines, livebearers and Hence the aspect of host-switching over larger phylo- killifishes [1–3], are well known ornamental fishes. genetic distances was not looked into. Moreover, Pari- American representatives like xiphos (Xiphophorus selle et al. [19, 31] raised the question of the origin Heckel, 1848) and guppies (Poecilia Bloch & Schneider, of Cichlidogyrus spp. described from cichlid hosts in 1801) have been adopted as model species featuring in Africa. Based on fossil, genetic and parasitic evidence, an increasing number of laboratory studies [4–6]. This is the authors hypothesized that cichlids may have origi- also the case for some African representatives, such as nated from Madagascar [37, 38] after the Gondwanan split species belonging to Nothobranchius Peters, 1868 [7–10]. and subsequently dispersed over Africa, Central and South They are also established models in ecology and evolu- America, India and the Middle East across various marine tionary biology [11–16] and parasitology [17, 18]. pathways [31, 38–40]. In this case, these teleosts would Evolutionary-parasitological research on these fishes often have encountered salinities that resulted in the loss of their deals with monogeneans, a species-rich clade of mostly ectoparasitic monogeneans (probably representatives of ectoparasitic flatworms. Fish-monogenean systems are Malagasy Insulacleidus Rakotofiringa & Euzet [41] or established models to study the evolution of host-parasite one of their ancestors) which show a poor tolerance interactions (e.g. [19, 20]). A diverse fauna of gyrodactylid to salinity and osmotic variations [31]. It is then likely monogeneans has been described from cyprinodontiform that cichlids, after reaching the African continent, hosts in both the Neotropics [21] and Africa [22]. The first have been newly colonized by an ancestor species of dactylogyridean monogenean parasites from African Cichlidogyrus, presumably transferred from a cur- cyprinodonts were described by Birgi and Euzet [23] on rently unspecified African fish. From there, the ances- the gills of some species of Aphyosemion Myers, 1924 tor of Cichlidogyrus evolved and specialized on sampled in different localities [Kala, Zamakoe and members of Cichlidae [26], and became host-specific Yaoundé (Central Region)] in Cameroon. Members of this (i.e. oioxenous [42]). As C. amieti is known to infect fish genus in general inhabit narrow, shallow and slowly- representatives of Cyprinodontiformes, it could be flowing forest streams [3, 24]. One of these killifish mono- possible that these fish represent the origin of the genean species, Cichlidogyrus amieti Birgi & Euzet [23], first host-switch to cichlids from which the present- was isolated from the gills of Aphyosemion cameronense day species-rich assemblage of Cichlidogyrus spp. on (Boulenger, 1903) and Aphyosemion obscurum (Ahl, old world cichlids arose. Indeed, similar radiation epi- 1924), two related species [2]. This discovery raised ques- sodes following a switch to a new host family have tions regarding the specificity of species belonging to been identified in monogeneans, for example in Gyro- Cichlidogyrus Paperna [25]. Indeed, no representative of dactylus [43]. In gyrodactylids, host-switching is even Cichlidogyrus had, at that time, ever been collected from a considered an important speciation mechanism [44]. fish not belonging to Cichlidae [26]. Birgi and Euzet [23] It has been suggested for a range of monogeneans therefore hypothesized that the presence of C. amieti on that colonization of different hosts is associated with the above mentioned two African cyprinodonts was prob- morphological adaptations, in particular to the attach- ably the result of a lateral transfer from cichlid fishes. ment organ ([45] and references therein). However, Switches to new host species represent a substantial risk morphological analysis linked the structure of hap- to, e.g., aquaculture and fisheries [27, 28]. They are also of toral hard parts in Cichlidogyrus to phylogenetic ra- fundamental