Maarten Van Steenberge

Ancyrocephalidae (Monogenea) of Lake Tanganyika. III : Cichlidogyrus infecting the world's biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae)

Lake Tanganyika is the deepest and oldest African Great Lake and of economic importance. While the diversity of its endemic cichlid radiations yielded scientific interest, a number of cichlid tribes have few representatives in the lake. Some of those, namely Oreochromini (ex-Tilapiini), Haplochromini and Tylochromini, reach higher species numbers in riverine systems. Conversely, the phylogenetic position of the monospecific and endemic Boulengerochromini is unclear. The oreochromines Oreochromis tanganicae and Oreochromis niloticus, the haplochromine Astatotilapia burtoni, the tylochromine Tylochromis polylepis and the boulengerochromine Boulengerochromis microlepis, the largest cichlid species worldwide, were surveyed for ancyrocephalid monogenean gill parasites. Five new species are proposed. Cichlidogyrus gillardinae sp. n. is described from A. burtoni, Cichlidogyrus mbirizei sp. n. from O. tanganicae and Cichlidogyrus nshomboi sp. n. from B. microlepis. T. polylepis harbours Cichlidogyrus mulimbwai sp. n., Cichlidogyrus muzumanii sp. n. and a third, presently undescribed species. Four species known from outside the Tanganyika Basin were retrieved on the oreochromines. The host species are scientific models or important in the sectors of fisheries or ornamental fish trade. Moreover, their phylogenetic positions render them well-suited to help elucidate the historic relationships between riverine and lacustrine African cichlids. In this framework, their Cichlidogyrus fauna is compared to congeners known from African rivers and to the few Tanganyika representatives described. While the parasites of Oreochromis, A. burtoni and T. polylepis are reminiscent of those infecting related hosts throughout Africa, B. microlepis hosts a Cichlidogyrus morphotype typical of Lake Tanganyika. This supports its placement within an endemic cichlid radiation.

Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites

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.

Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus

BackgroundAdaptation to different ecological environments is thought to drive ecological speciation. This phenomenon culminates in the radiations of cichlid fishes in the African Great Lakes. Multiple characteristic traits of cichlids, targeted by natural or sexual selection, are considered among the driving factors of these radiations. Parasites and pathogens have been suggested to initiate or accelerate speciation by triggering both natural and sexual selection. Three prerequisites for parasite-driven speciation can be inferred from ecological speciation theory. The first prerequisite is that different populations experience divergent infection levels. The second prerequisite is that these infection levels cause divergent selection and facilitate adaptive divergence. The third prerequisite is that parasite-driven adaptive divergence facilitates the evolution of reproductive isolation. Here we investigate the first and the second prerequisite in allopatric chromatically differentiated lineages of the rock-dwelling cichlid Tropheus spp. from southern Lake Tanganyika (Central Africa). Macroparasite communities were screened in eight populations belonging to five different colour morphs.ResultsParasite communities were mainly composed of acanthocephalans, nematodes, monogeneans, copepods, branchiurans, and digeneans. In two consecutive years (2011 and 2012), we observed significant variation across populations for infection with acanthocephalans, nematodes, monogeneans of the genera Gyrodactylus and Cichlidogyrus, and the copepod Ergasilus spp. Overall, parasite community composition differed significantly between populations of different colour morphs. Differences in parasite community composition were stable in time. The genetic structure of Tropheus populations was strong and showed a significant isolation-by-distance pattern, confirming that spatial isolation is limiting host dispersal. Correlations between parasite community composition and Tropheus genetic differentiation were not significant, suggesting that host dispersal does not influence parasite community diversification.ConclusionsSubject to alternating episodes of isolation and secondary contact because of lake level fluctuations, Tropheus colour morphs are believed to accumulate and maintain genetic differentiation through a combination of vicariance, philopatric behaviour and mate discrimination. Provided that the observed contrasts in parasitism facilitate adaptive divergence among populations in allopatry (which is the current situation), and promote the evolution of reproductive isolation during episodes of sympatry, parasites might facilitate speciation in this genus.

A recent inventory of the fishes of the north-western and central western coast of Lake Tanganyika (Democratic Republic Congo)

Background. Despite the importance of Lake Tanganyikas biodiversity for science and the livelihoods of the riparian people, high-resolution surveys of the fish biodiversity are sparse and fragmentary, especially along the western (Congolese) shoreline. The coast suffers locally from intensive human activities and lacks adequate protective measures or nature reserves. However, in view of the intra-lacustrine endemism of this fish fauna, conservation needs to be managed lake-wide at a fine scale, necessitating detailed inventories on fish species distribution. The study aims at updating knowledge on fish diversity and distribution along the north-western and central western shores of Lake Tanganyika. Materials and methods. Fish specimens were collected using gill-and seine nets, by snorkelling and SCUBA diving, and through purchases on the local markets. Results. Over 28 locations were sampled, and 84 cichlid- and 30 non-cichlid fish species (belonging to Protopteridae, Clupeidae, Cyprinidae, Alestidae, Claroteidae, Clariidae, Malapteruridae, Mochokidae, Poeciliidae, Latidae, and Mastacembelidae) collected. Conclusion. Our records substantially expand the known range of fish species in a range of habitats. As numerous specimens are hard to assign to nominal species, a taxonomic revision of a number of genera is underway. It should take into account intraspecific geographic variation.

Morphology, Molecules, and Monogenean Parasites: An Example of an Integrative Approach to Cichlid Biodiversity

The unparalleled biodiversity of Lake Tanganyika (Africa) has fascinated biologists for over a century; its unique cichlid communities are a preferred model for evolutionary research. Although species delineation is, in most cases, relatively straightforward, higher-order classifications were shown not to agree with monophyletic groups. Here, traditional morphological methods meet their limitations. A typical example are the tropheine cichlids currently belonging to Simochromis and Pseudosimochromis. The affiliations of these widespread and abundant cichlids are poorly understood. Molecular work suggested that genus and species boundaries should be revised. Moreover, previous morphological results indicated that intraspecific variation should be considered to delineate species in Lake Tanganyika cichlids. We review the genera Simochromis and Pseudosimochromis using an integrative approach. Besides a morphometric study and a barcoding approach, monogenean Cichlidogyrus (Platyhelminthes: Ancyrocephalidae) gill parasites, often highly species-specific, are used as complementary markers. Six new species are described. Cichlidogyrus raeymaekersi sp. nov., C. muterezii sp. nov. and C. banyankimbonai sp. nov. infect S. diagramma. Cichlidogyrus georgesmertensi sp. nov. was found on S. babaulti and S. pleurospilus, C. franswittei sp. nov. on both S. marginatus and P. curvifrons and C. frankwillemsi sp. nov. only on P. curvifrons. As relatedness between Cichlidogyrus species usually reflects relatedness between hosts, we considered Simochromis monotypic because the three Cichlidogyrus species found on S. diagramma belonged to a different morphotype than those found on the other Simochromis. The transfer of S. babaulti, S. marginatus, S. pleurospilus and S. margaretae to Pseudosimochromis was justified by the similarity of their Cichlidogyrus fauna and the intermediate morphology of S. margaretae. Finally parasite data also supported the synonymy between S. pleurospilus and S. babaulti, a species that contains a large amount of geographical morphological variation.

Ancyrocephalidae (Monogenea) of Lake Tanganyika: IV: Cichlidogyrus parasitizing species of Bathybatini (Teleostei, Cichlidae): reduced host-specificity in the deepwater realm?

Abstract Lake Tanganyika’s biodiversity and endemicity sparked considerable scientific interest. Its monogeneans, minute parasitic flatworms, have received renewed attention. Their host-specificity and simple life cycle render them ideal for parasite speciation research. Because of the wide ecological and phylogenetic range of its cichlids, Lake Tanganyika is a “natural experiment” to contrast factors influencing monogenean speciation. Three representatives of Bathybatini (Bathybates minor, B. fasciatus, B. vittatus), endemic predatory non-littoral cichlids, host a single dactylogyridean monogenean species. It is new to science and described as Cichlidogyrus casuarinus sp. nov. This species and C. nshomboi and C. centesimus, from which it differs by the distal end of the accessory piece of the male apparatus and the length of its heel, are the only Cichlidogyrus species with spirally coiled thickening of the penis wall. In Cichlidogyrus, this feature was only found in parasites of endemic Tanganyika tribes. The seemingly species-poor Cichlidogyrus community of Bathybatini may be attributed to meagre host isolation in open water. The new species infects cichlids that substantially differ phylogenetically and ecologically. This may be an adaptation to low host availability. Cichlidogyrus species infecting African Great Lake cichlids are summarized and proposed as model for the influence of host ecology on disease transmission.

Complex geographical variation patterns in Tropheus duboisi Marlier, 1959 (Perciformes, Cichlidae) from Lake Tanganyika

Intra-specific morphological variation in the cichlid Tropheus duboisi from 10 localities over its entire known distribution area along the central eastern and northern shore of Lake Tanganyika was investigated. This revealed significant differences between various populations that are geographically isolated. These morphological observations only partially correspond to the results of a haplotype network, based on mtDNA. In addition, a difference in the timing of the onset of the adult colour pattern was discovered for one isolated population. The occurrence of morphological intra-specific differentiation is discussed with respect to the basal position of T. duboisi within Tropheus as well as to the presumed morphological stasis of the genus.

Biogeographical implications of Zambezian Cichlidogyrus species (Platyhelminthes: Monogenea: Ancyrocephalidae) parasitizing Congolian cichlids

Fishes normally restricted to inland waters are valuable model systems for historical biogeography, inter alia, because of their limited dispersal abilities and concordance with the distribution patterns of other freshwater taxa (Zogaris et al. 2009). The comparison of fish species assemblages has been the major biogeographical tool for delineating African aquatic ecoregions as the fossil record is often meagre and merely offers complementary information. This is, for example, the case for the Zambezian and Congolian ichthyofaunal provinces, which display substantial contemporary fish diversity (Stewart 2001). Between both regions lies the Bangweulu-Mweru ecoregion (sensu Scott 2005), known for its high percentage of endemicity. Although hydrographically belonging to the Congo Basin, the Bangweulu-Mweru ecoregion has a high affinity with the Zambezi province (Scott 2005), due to historical river connections (Tweddle 2010). Studies comparing the Zambezi and Congo ichthyofaunal provinces are rare and hampered by lack of data from the Congo Basin. The latter harbours more than 1250 fish species (Snoeks et al. 2011) while in the Zambezi, only 120 freshwater fishes are found (Tweddle 2010). Indeed, species richness declines in all major African teleost families from the Congo Basin southwards, riverine haplochromine cichlids forming a notable exception to this rule (Joyce et al. 2005). Although it was hypothesized by Tweddle (2010) that the origin of many Zambezian fish species is in the Congo Basin, the haplochromines Serranochromis Regan, Sargochromis Regan, Pharyngochromis Greenwood and Chetia Trewavas, together forming the serranochromines, have their centre of diversity in the rivers of the Zambezian ichthyofaunal province (Joyce et al. 2005). Therefore, the biogeographical history of Cichlidae across the Zambezi- Congo watershed is not only key to cichlid biogeography on an African scale, but also complementary to biogeography of all other teleosts in the region. Yet, colonisation and speciation patterns are difficult to unravel due to complex hydrological history (Katongo et al. 2007; Schwarzer et al. 2012).

Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus

Stenotopic specialization to a fragmented habitat promotes the evolution of genetic structure. It is not yet clear whether small-scale population structure generally translates into large-scale intraspecific divergence. In the present survey of mitochondrial genetic structure in the Lake Tanganyika endemic Altolamprologus (Teleostei, Cichlidae), a rock-dwelling cichlid genus comprising A. compressiceps and A. calvus, habitat-induced population fragmentation contrasts with weak phylogeographic structure and recent divergence among genetic clades. Low rates of dispersal, perhaps along gastropod shell beds that connect patches of rocky habitat, and periodic secondary contact during lake level fluctuations are apparently sufficient to maintain genetic connectivity within each of the two Altolamprologus species. The picture of genetic cohesion was interrupted by a single highly divergent haplotype clade in A. compressiceps restricted to the northern part of the lake. Comparisons between mitochondrial and nuclear phylogenetic reconstructions suggested that the divergent mitochondrial clade originated from ancient interspecific introgression. Finally, ‘isolation-with-migration’ models indicated that divergence between the two Altolamprologus species was recent (67–142 KYA) and proceeded with little if any gene flow. As in other rock-dwelling cichlids, recent population expansions were inferred in both Altolamprologus species, which may be connected with drastic lake level fluctuations.

Testing the potential of DNA barcoding in vertebrate radiations: the case of the littoral cichlids (Pisces, Perciformes, Cichlidae) from Lake Tanganyika

We obtained 398 cytochrome c oxidase subunit I barcodes of 96 morphospecies of Lake Tanganyika (LT) cichlids from the littoral zone. The potential of DNA barcoding in these fishes was tested using both species identification and species delineation methods. The best match (BM) and best close match (BCM) methods were used to evaluate the overall identification success. For this, three libraries were analysed in which the specimens were categorized into Operational Taxonomic Units (OTU) in three alternative ways: (A) morphologically distinct, including undescribed, species, (B) valid species and (C) complexes of morphologically similar or closely related species. For libraries A, B and C, 73, 73 and 96% (BM) and 72, 70 and 94% (BCM) of the specimens were correctly identified. Additionally, the potential of two species delineation methods was tested. The General Mixed Yule Coalescent (GMYC) analysis suggested 70 hypothetical species, while the Automatic Barcode Gap Discovery (ABGD) method revealed 115 putative species. Although the ABGD method had a tendency to oversplit, it outperformed the GMYC analysis in retrieving the species. In most cases where ABGD suggested oversplitting, this was due to intraspecific geographical variation. The failure of the GMYC method to retrieve many species could be attributed to discrepancies between mitochondrial gene trees and the evolutionary histories of LT cichlid species. Littoral LT cichlids have complex evolutionary histories that include instances of hybridization, introgression and rapid speciation. Nevertheless, although the utility of DNA barcoding in identification is restricted to the level of complexes, it has potential for species discovery in cichlid radiations.