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

Mandeng, Françoise D. Messu; Bilong, Charles Félix Bilong; Pariselle, Antoine; Vanhove, Maarten Pieterjan; Nyom, Arnold R. Bitja; Agnèse, Jean‐François

doi:10.1186/s13071-015-1181-y

Cited by 57 publications

(79 citation statements)

References 76 publications

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“…3, Table 3), no structural morphological difference except a size difference was seen in the MCO. This discrepancy has been previously reported in other monogenean species belonging to Pseudorhabdosynochus Yamaguti, 1958 (Sigura and Justine, 2008) and Cichlidogyrus (Messu Mandeng et al, 2015). This is supposed to be influenced by the degree of host genetic differentiation correlated with the age of the parasite lineage (Poulin, 1992(Poulin, , 2007Poulin and Morand, 2004).…”

Section: Intra-specific Morphological Variabilitymentioning

confidence: 70%

Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability

Kmentová

Steenberge

Raeymaekers

et al. 2018

CTOZ

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Whereas Lake Tanganyika's littoral and benthic zones are famous for their diverse fish communities, its pelagic zone is dominated by few species, of which two representatives of Clupeidae (Limnothrissa miodon and Stolothrissa tanganicae) take a pivotal role. We investigated the monogenean fauna infecting these freshwater clupeids to explore the link between parasite morphology and host species identity, or seasonal and geographical origin, which may reveal host population structure. Furthermore, we conducted phylogenetic analyses to test whether these parasitic flatworms mirror their host species' marine origin. Based on 406 parasite specimens infecting 385 host specimens, two monogenean species of Kapentagyrus Kmentová, Gelnar and Vanhove, gen. nov. were morphologically identified and placed in the phylogeny of Dactylogyridae using three molecular markers. One of the species, Kapentagyrus limnotrissae comb. nov., is host-specific to L. miodon while its congener, which is new to science and described as Kapentagyrus tanganicanus Kmentová, Gelnar and Vanhove, sp. nov., is infecting both clupeid species. Morphometrics of the parasites' hard parts showed intra-specific variability, related to host species identity and seasonality in K. tanganicanus. Significant intra-specific differences in haptor morphometrics between the northern and southern end of Lake Tanganyika were found, and support the potential use of monogeneans as tags for host population structure. Based on phylogenetic inference, we suggest a freshwater origin of the currently known monogenean species infecting clupeids in Africa, with the two species from Lake Tanganyika representing a quite distinct lineage.

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Section: Intra-specific Morphological Variabilitymentioning

confidence: 70%

Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability

Kmentová

Steenberge

Raeymaekers

et al. 2018

CTOZ

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“… Morand et al (2002) assume that haptoral structures do not reflect a phylogenetic pattern as a result of adaptation to microhabitat within the host. Moreover, Messu Mandeng et al (2015) point out an adaptive component in the attachment organ morphology of Cichlidogyrus . However, other studies suggest the existence of a phylogenetic signal in sclerite morphology and shape within dactylogyridean monogeneans ( Šimková et al, 2002 ; Šimková et al, 2006 ) and specifically within Cichlidogyrus ( Vignon, Pariselle & Vanhove, 2011 ).…”

Section: Discussionmentioning

confidence: 95%

First insights into the diversity of gill monogeneans of‘Gnathochromis’andLimnochromis(Teleostei, Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history?

Kmentová

Gelnar

Koblmüller

et al. 2016

PeerJ

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Monogenea is one of the most species-rich groups of parasitic flatworms worldwide, with many species described only recently, which is particularly true for African monogeneans. For example, Cichlidogyrus, a genus mostly occurring on African cichlids, comprises more than 100 nominal species. Twenty-two of these have been described from Lake Tanganyika, a famous biodiversity hotspot in which many vertebrate and invertebrate taxa, including monogeneans, underwent unique and spectacular radiations. Given their often high degrees of host specificity, parasitic monogeneans were also used as a potential tool to uncover host species relationships. This study presents the first investigation of the monogenean fauna occurring on the gills of endemic ‘Gnathochromis’ species along the Burundese coastline of Lake Tanganyika. We test whether their monogenean fauna reflects the different phylogenetic position and ecological niche of ‘Gnathochromis’ pfefferi and Gnathochromis permaxillaris. Worms collected from specimens of Limnochromis auritus, a cichlid belonging to the same cichlid tribe as G. permaxillaris, were used for comparison. Morphological as well as genetic characterisation was used for parasite identification. In total, all 73 Cichlidogyrus individuals collected from ‘G.’ pfefferi were identified as C. irenae. This is the only representative of Cichlidogyrus previously described from ‘G.’ pfefferi, its type host. Gnathochromis permaxillaris is infected by a species of Cichlidogyrus morphologically very similar to C. gillardinae. The monogenean species collected from L. auritus is considered as new for science, but sample size was insufficient for a formal description. Our results confirm previous suggestions that ‘G.’ pfefferi as a good disperser is infected by a single monogenean species across the entire Lake Tanganyika. Although G. permaxillaris and L. auritus are placed in the same tribe, Cichlidogyrus sp. occurring on G. permaxillaris is morphologically more similar to C. irenae from ‘G.’ pfefferi, than to the Cichlidogyrus species found on L. auritus. Various evolutionary processes, such as host-switching or duplication events, might underlie the pattern observed in this particular parasite-host system. Additional samples for the Cichlidogyrus species occuring on G. permaxillaris and L. auritus are needed to unravel their evolutionary history by means of (co-)phylogenetic analyses.

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“…On the other hand, in Cichlidogyrus (Family: Ancyrocephalidae), sclerite (including anchors) shape was found to contain significant phylogenetic signal ( Vignon, Pariselle & Vanhove, 2011 ). However, this conclusion needs to be qualified in light of the recent demonstration of a host-switching event in Cichlidogyrus ( Messu Mandeng et al, 2015 ), which was missed in Vignon, Pariselle & Vanhove (2011) because the host range (at the familial level of the fish hosts) of Cichlidoygrus was not taken into consideration. For Ligophorus , the significant phylogenetic signal found in the anchors does not appear to need similar qualification, since its host range is currently known to be restricted to mullets.…”

Section: Discussionmentioning

confidence: 99%

Monogenean anchor morphometry: systematic value, phylogenetic signal, and evolution

Khang

Soo

Tan

et al. 2016

PeerJ

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Background. Anchors are one of the important attachment appendages for monogenean parasites. Common descent and evolutionary processes have left their mark on anchor morphometry, in the form of patterns of shape and size variation useful for systematic and evolutionary studies. When combined with morphological and molecular data, analysis of anchor morphometry can potentially answer a wide range of biological questions.Materials and Methods. We used data from anchor morphometry, body size and morphology of 13 Ligophorus (Monogenea: Ancyrocephalidae) species infecting two marine mugilid (Teleostei: Mugilidae) fish hosts: Moolgarda buchanani (Bleeker) and Liza subviridis (Valenciennes) from Malaysia. Anchor shape and size data (n = 530) were generated using methods of geometric morphometrics. We used 28S rRNA, 18S rRNA, and ITS1 sequence data to infer a maximum likelihood phylogeny. We discriminated species using principal component and cluster analysis of shape data. Adams’s Kmult was used to detect phylogenetic signal in anchor shape. Phylogeny-correlated size and shape changes were investigated using continuous character mapping and directional statistics, respectively. We assessed morphological constraints in anchor morphometry using phylogenetic regression of anchor shape against body size and anchor size. Anchor morphological integration was studied using partial least squares method. The association between copulatory organ morphology and anchor shape and size in phylomorphospace was used to test the Rohde-Hobbs hypothesis. We created monogeneaGM, a new R package that integrates analyses of monogenean anchor geometric morphometric data with morphological and phylogenetic data.Results. We discriminated 12 of the 13 Ligophorus species using anchor shape data. Significant phylogenetic signal was detected in anchor shape. Thus, we discovered new morphological characters based on anchor shaft shape, the length between the inner root point and the outer root point, and the length between the inner root point and the dent point. The species on M. buchanani evolved larger, more robust anchors; those on L. subviridis evolved smaller, more delicate anchors. Anchor shape and size were significantly correlated, suggesting constraints in anchor evolution. Tight integration between the root and the point compartments within anchors confirms the anchor as a single, fully integrated module. The correlation between male copulatory organ morphology and size with anchor shape was consistent with predictions from the Rohde-Hobbs hypothesis.Conclusions. Monogenean anchors are tightly integrated structures, and their shape variation correlates strongly with phylogeny, thus underscoring their value for systematic and evolutionary biology studies. Our MonogeneaGM R package provides tools for researchers to mine biological insights from geometric morphometric data of speciose monogenean genera.

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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

Cited by 57 publications

References 76 publications

Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability

Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability

First insights into the diversity of gill monogeneans of‘Gnathochromis’andLimnochromis(Teleostei, Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history?

Monogenean anchor morphometry: systematic value, phylogenetic signal, and evolution

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