PERMANENT GENETIC RESOURCES: Isolation and characterization of microsatellite loci in the cichlid fish in Lake Victoria, Haplochromis chilotes

Twelve short tandem repeat markers were successfully isolated from a cichlid, Haplochromis chilotes, in Lake Victoria, and characterized in Haplochromis pyrrhocephalus. The microsatellite regions of these markers were found to have between two and 48 alleles with heterozygosity ranging from 0.07 to 0.97. No loci showed significant departures from the Hardy–Weinberg or linkage equilibrium after the Bonferroni correction (P > 0.05). Cross‐species amplification in other cichlids of Lake Victoria, Haplochromis laparogramma, Lithochromis rubripinnis, L. rufus and Haplochromis sp. ‘rockkribensis’, was successful.     

Species specificity and sexual dimorphism in tooth shape among the three sympatric haplochromine species in Lake Kivu cichlids

Tooth shape is used to differentiate between morphologically similar species of vertebrates, including fish. This study aimed to quantify tooth shape of three sympatric species: Haplochromis kamiranzovu, H. insidiae, and H. astatodon endemic to Lake Kivu, whose existing identification criteria are currently only qualitative. A quantitative tooth shape analysis was performed based on digitized tooth outline data with a subsequent elliptic Fourier analysis to test for differences among the three species. We looked at crown shape and size differences within H. kamiranzovu and H. insidiae at geographical, habitat, and gender levels. No comparison at habitat level was done for H. astatodon because it is found only in littoral zone. The analysis revealed significant tooth shape differences among the three species. Haplochromis astatodon had a significantly longer major cusp height and a longer and larger minor cusp than that of H. insidiae. It had also a longer major cusp height and a longer and larger minor cusp than that of H. kamiranzovu. Tooth shape differences of H. kamiranzovu and H. insidiae species were not significantly different between littoral and pelagic fish (p > .05) while differences were significant between southern and northern Lake Kivu populations (p < .05). Tooth sizes in H. kamiranzovu and H. insidiae were significantly different, both in height and width as well as in their ratios, and this was true at sex and geographic levels (p < .05), but not at habitat level (p > .05). Tooth shape was also significantly different with sharp teeth for males compared with females of southern populations versus northern ones. These shape‐ and size‐related differences between sexes suggest differences in the foraging strategies toward available food resources in the lake habitat. Further research should explain the genetic basis of the observed pattern.     

The synonymy of Haplochromis pharyngalis and Haplochromis petronius (Cichlidae)

Haplochromis pharyngalis and Haplochromis petronius, two endemic cichlids from the Lake Edward system (Uganda, Democratic Republic of the Congo), are very similar in general morphology but have been reported to differ in pharyngeal jaw morphology and distribution. This study analysed 51 morphometrics and various qualitative characteristics of 48 specimens from different localities. The morphological traits of both species strongly overlap, and differences in the pharyngeal jaw morphology correspond to a geographic morphocline. We conclude that all specimens belong to one valid species, H. pharyngalis, and consider H. petronius to be a synonym.     

An annotated checklist of the fish fauna of the river systems draining the Kahuzi-Biega National Park (Upper Congo: Eastern DR Congo)

The Kahuzi-Biega National Park (KBNP), situated mainly in the Eastern Highlands Ecoregion of the Upper Congo basin, is drained by the Lowa and Ulindi rivers, and some western affluents of Lake Kivu. In this study, the first list of the fish diversity of these systems is provided based on museum collections and complemented, for the Lowa River system and the western Lake Kivu affluents, with recently collected specimens (2013–2017). A total of 118 species are reported from the Lowa basin, 22 from the Ulindi basin and seven from these Lake Kivu affluents. Within the Lowa and Ulindi, respectively, five and one species, all cichlids, have been introduced. Currently, 51 species are reported from within the park, only two of which have been reported from the highlands, i.e., Amphilius kivuensis from the Luha, the source of the Luka River, and Clarias liocephalus from the headwaters of the Lake Kivu’ affluents. With a total of 30 species, Cyprinidae is by far the largest family, representing 25% of the total species diversity of the Lowa basin. It is followed by Mormyridae with 13 species (11%), Alestidae and Mochokidae with 10 species each (8%), Clariidae and Amphiliidae with eight species (7%), and Distichodontidae with six species (5%). Seven new species for science were discovered and 11 species were found to be endemic to the Lowa system. Although further exploration is needed, this underscores the importance of the KBNP in protecting the fish fauna of the Lowa basin but also highlights the park's limited coverage of the fish fauna of the Lowa basin.     

Structural genomic variation leads to genetic differentiation in Lake Tanganyika's sardines

Identifying patterns in genetic structure and the genetic basis of ecological adaptation is a core goal of evolutionary biology and can inform the management and conservation of species that are vulnerable to population declines exacerbated by climate change. We used reduced‐representation genomic sequencing methods to gain a better understanding of genetic structure among and within populations of Lake Tanganyika's two sardine species, Limnothrissa miodon and Stolothrissa tanganicae. Samples of these ecologically and economically important species were collected across the length of Lake Tanganyika, as well as from nearby Lake Kivu, where L. miodon was introduced in 1959. Our results reveal differentiation within both S. tanganicae and L. miodon that is not explained by geography. Instead, this genetic differentiation is due to the presence of large sex‐specific regions in the genomes of both species, but involving different polymorphic sites in each species. Our results therefore indicate rapidly evolving XY sex determination in the two species. Additionally, we found evidence of a large chromosomal rearrangement in L. miodon, creating two homokaryotypes and one heterokaryotype. We found all karyotypes throughout Lake Tanganyika, but the frequencies vary along a north–south gradient and differ substantially in the introduced Lake Kivu population. We do not find evidence for significant isolation by distance, even over the hundreds of kilometres covered by our sampling, but we do find shallow population structure.     

Midwater spawning inHaplochromis chrysonotus (Boulenger) (Teleostei: Cichlidae) in Lake Malawi

Synopsis Haplochromis chrysonotus, a semipelagic shoaling cichlid from Lake Malawi, has been observed spawning in open water up to ten metres above the substratum. It is suggested that open water spawning without the establishment of a substratum-based territory eliminates competition with other species for breeding space and that it may be a stage in the evolution of a totally pelagic mode of life.     

Diet overlap between the newly introduced <Emphasis Type="Italic">Lamprichthys tanganicanus</Emphasis> and the Tanganyika sardine in Lake Kivu,Eastern Africa

This study evaluates the possible competition for food between Lamprichthys tanganicanus, recently introduced in Lake Kivu, and Limnothrissa miodon, which has been the basis of the pelagic fishery in this lake for several decades. Since 2006, L. tanganicanus has expanded in the lake and its numbers have increased in the captures, raising concern for the sardine fishery. We carried out a 2-year monthly survey, based on experimental captures in littoral and pelagic stations, which demonstrated the invasive dispersal of L. tanganicanus in littoral and pelagic waters. The diet of both species was determined on the basis of gut content analyses, taking into account the influence of site and season, and a diet overlap index was calculated. In the pelagic zone, where almost all size classes of both species were present and essentially fed upon mesozooplankton, the diet overlap was high. This situation stems from the fact that L. tanganicanus has colonized the pelagic zone in Lake Kivu, likely in search for more abundant mesozooplankton. Inshore, the diet overlap between the two species was lower, as L. tanganicanus consumed a broad range of food, whereas L. miodon strongly selected insects and, chiefly for the largest specimens, fishes. These results suggest a likelihood of interspecific competition, particularly offshore, where mesozooplankton is the main available food type, and call for further monitoring of the sardine fishery, to assess a possible impact of the invader.     

Biology of the African clupeid Limnothrissa miodon with reference to its small size in artificial lakes

Summary Limnothrissa miodon is a clupeid from Lake Tanganyika which has been introduced to Lakes Kivu and Kariba and which invaded Lake Cahora Bassa. These lakes differ considerably from one another but the biology of Limnothrissa is similar in many respects in all of them. Similarities include its feeding and breeding biology, whilst its populations fluctuate, on both an annual and a seasonal basis, in relation to environmental changes. The major differences between the lakes concern the size to which Limnothrissa grows. Their average length in the two natural lakes, Lakes Tanganyika and Kivu, is about twice the average length in the two artificial lakes, Lakes Kariba and Cahora Bassa. This in turn affects their age of maturity and they breed during their first year in the reservoirs but during their second in the natural lakes. Their growth rates and performance are comparable up to about 6 months of age and the difference in their size seems to be due to high mortality in the artificial lakes where few Limnothrissa survive for more than a year. Possible explanations for their small size include the genetic composition of the original introduction and the unpredictability of the environment. Neither of these explanations is supported by evidence at present. Deficiencies in the available food and the effects of intense predation are probably the most likely causes. In both natural lakes, Limnothrissa are predatory or cannibalistic from 100 mm in length and 12 months in age, and fish in their diet may enable them to survive into their second year. The fish in Lakes Kariba and Cahora Bassa, in contrast, are neither predatory nor cannibalistic to any degree. There are no predatory fish species in Lake Kivu but there is a diverse community of pelagic piscivores in Lake Tanganyika which tends to contradict the predation hypothesis. However, the position of Limnothrissa in the reservoirs probably resembles that occupied in Lake Tanganyika by Stolothrissa which is also a small, annual species. The significance of this phenomenon is that Limnothrissa can maintain a high biomass and productivity in the face of intense predation. This trait may be of importance to fisheries management because it means that their yield can be greatly increased.     

Phylogeography and Evolution of the Tanganyikan Cichlid Genus Tropheus Based upon Mitochondrial DNA Sequences

Abstract Lake Tanganyika harbors the oldest and most diverse species flock of cichlid fish. Many species are subdivided into numerous genetically and phenotypically distinct populations. Their present distribution and genetic structure were shaped by a series of lake level fluctuations which caused cycles of isolation and admixis and promoted dispersal events. One of the best examples of this phenomenon is the genus Tropheus. We present a comprehensive mtDNA phylogeny based upon 365 individuals of 55 populations from all over Lake Tanganyika, which suggests an almost-contemporaneous origin of eight major mitochondrial lineages about 700 Ka ago. While the distribution of seven lineages is restricted to particular sections of the lake shore, one lineage was found to have a much more widespread distribution. This particular lineage is subdivided into four sublineages which seem to have originated from a single dispersal event about 400 Ka. By using a molecular clock estimate in combination with geological data we derived a hypothetical scenario for the colonization history of Tropheus. Thereby we show a high degree of concordance between major changes of the lake level in the recent history of Lake Tanganyika and three distinct diversification events in this genus.     

Comparative rates of lower jaw diversification in cichlid adaptive radiations

The lower jaw (LJ) provides an ideal trophic phenotype to compare rates and patterns of macroevolution among cichlid radiations. Using a novel phylogeny of four genes (ND2, dlx2, mitfb, and s7), we examined the evolutionary relationships among two of the most phylogenetically disparate cichlid radiations: (i) the Central America Heroines; and (ii) the East African Lake Malawi flock. To quantify jaw morphology, we measured two LJ lever systems in approximately 40 species from each lineage. Using geologic calibrations, we generated a chronogram for both groups and examined the rates of jaw evolution in the two radiations. The most rapidly evolving components of the LJ differed between the two radiations. However, the Lake Malawi flock exhibited a much faster rate of evolution in several components of the LJ. This rapid rate of divergence is consistent with natural selection, promoting unparalleled trophic diversification in Lake Malawi cichlids.     

Similar ecology,different morphology: Three new species of oral-mollusc shellers from Lake Edward

Lake Edward, East Africa, harbours a largely understudied assemblage of haplochromine cichlids that displays a range of adaptions to various specialised trophic niches. In this system, we discovered specimens of Haplochromis with morphologies similar to those of oral-mollusc shellers from Lake Victoria. These morphologies are characterised by short oral jaws with stout teeth that are used either to crush molluscs or to grab the soft bodies of snails and wrench them out of their shells. A morphometric study on 47 specimens from Lake Edward revealed the presence of three new species with an oral-shelling morphology: Haplochromis concilians sp. nov., H. erutus sp. nov. and H. planus sp. nov. All three species are formally described. Stomach-content observations confirmed an opportunistic oral-shelling ecology for H. concilians sp. nov. and H. erutus sp. nov. Within H. planus sp. nov., only large specimens displayed a specialised oral-shelling morphology, but their stomachs were nearly empty, while small specimens consumed mainly Ostracoda and Hydrachnidia. Remarkably, the three species differed considerably in morphology from each other, but they each resembled oral-sheller species from Lake Victoria.     

Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of lake Malawi, East Africa

Considerable controversy has surrounded the application of mitochondrial DNA data to reconstruction of evolutionary relationships among the endemic cichlids of Lake Malawi. Central to this debate has been the issue of whether lineage sorting is complete, and thus whether these data actually reflect species phylogeny, or simply gene genealogy. Review of all mtDNA control region sequences available for members of one monophyletic subset of this species flock, the Malawi rockfishes, or mbuna, strongly indicates that lineage sorting is incomplete: Character-based analyses of these sequences reconstruct gene, not species, interrelationships. Analysis of the pattern of nucleotide substitutions differentiating these mtDNA alleles suggests that pyrimidine residues undergo transition substitutions more often than do purines. Estimation of the magnitude of derived sequence differentiation in light of the reconstructed gene genealogy suggests that the mbuna may be of considerably more recent vintage than previous molecular characterizations have indicated. Received: 6 April 1996 / Accepted: 3 March 1997     

MOLECULAR PHYLOGENY OF THE UPRIGHT ERYTHROPELTIDALES (COMPSOPOGONOPHYCEAE,RHODOPHYTA): MULTIPLE CRYPTIC LINEAGES OF ERYTHROTRICHIA CARNEA1

The phylogeny of morphologically simple algae is problematic due to insufficient morphological characters to aid in distinguishing species and relationships. The problem is further compounded because multiple evolutionary lineages of morphologically similar species occur in most well‐sampled biogeographic locations; therefore, location cannot be used as a proxy for species. The phylogeny of the upright members of the Erythropeltidales is partially clarified by combining molecular data, unialgal culture observations, and worldwide sampling. Our results show that there are several well‐supported lineages within the Erythropeltidales with only two morphologically recognizable taxa at present. The first is the genus Porphyrostromium, with a well‐developed basal crust, which includes two Erythrotrichia species (Porphyrostromium ligulatum comb. nov. and Porphyrostromium pulvinatum comb. nov.). The second is the branched species Erythrotrichia welwitschii (Rupr.) Batters. There are also six strongly supported Erythrotrichia carnea–like lineages. While not completely satisfactory, we propose that one lineage (lineage 2) with samples close to the type locality be designated as E. carnea with a specific isolate as an epitype. The lack of morphology to differentiate the other lineages leads to a taxonomy based solely on gene sequencing and molecular phylogeny, with rbcL sequences differentiating the lineages proposed. We hold off on proposing more species and genera until more data and samples can be gathered.     

Photopic adaptations to a changing environment in two Lake Victoria cichlids

During the past 30 years, Lake Victoria cichlid fishes have encountered severe environmental and ecological changes including an introduced predator and new prey types. Furthermore, increased eutrophication has led to reduced water transparency and shifted the spectral composition of underwater light to longer wavelengths. In the present study, collections of two cichlid species, Haplochromis pyrrhocephalus and Haplochromis tanaos, from before and after the environmental changes, were compared with respect to their photopic resolution and sensitivity. Eyes of both species were dissected and retinal features were measured from tangential sections. In both species, the eyes became smaller, independently of body size. This decrease possibly occurred to make space for other structures that increased in size. In H. pyrrhocephalus, a significantly lower resolution was found. However, the size, and thus photon‐catching ability of the double cones, remained unchanged, despite the smaller eyes. In the modern populations of H. tanaos, the double cone size increased in relation to eye size, so that the photon‐catching ability of the smaller fish remained the same. However, no significant decrease in resolution was found. Shortwave sensitivity was found to be lower in both modern populations because of a reduction or the complete absence of single cones. The results obtained in the present study imply that these resurgent zooplanktivores are capable of adapting their eye morphology to the changed environmental conditions without losing crucial aspects used for survival and reproduction. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 328–341.     

The effect of environmental diversification on species diversification in New Caledonian caddisflies (Insecta: Trichoptera: Hydropsychidae)

Aim To test whether environmental diversification played a role in the diversification of the New Caledonian Hydropsychinae caddisflies. Location New Caledonia, south‐west Pacific. Methods The phylogeny of the New Caledonian Hydropsychinae caddisflies was hypothesized using parsimony and Bayesian methods on molecular characters. The Bayesian analysis was the basis for a comparative analysis of the correlation between phylogeny and three environmental factors: geological substrate (ultrabasic, non‐ultrabasic), elevation and precipitation. Phylogenetic divergence times were estimated using a relaxed clock method, and environmental factors were mapped onto a lineage‐through‐time plot to investigate the timing of environmental diversification in relation to species radiation. The correlation between rainfall and elevation was tested using independent contrasts, and the gamma statistic was calculated to infer the diversification pattern of the group. Results The diversification of extant Orthopsyche–Caledopsyche species began in the Middle–Late Oligocene, when much of the island of New Caledonia was covered by ultrabasic substrate and mountain forming was prevalent. Most lineages originated in the Middle–Late Miocene, a period associated with long‐term climate oscillation. Optimization of environmental factors on the phylogeny demonstrated that the New Caledonian Hydropsychinae group adapted to ultrabasic substrate early in its evolutionary history. The clade living mostly on ultrabasic substrate was far more species‐rich than the clade living mostly on non‐ultrabasic substrate. Elevation and rainfall were significantly correlated with each other. The lineage‐through‐time plot revealed that the main environmental diversification preceded species diversification. A constant speciation through time was rejected, and the negative gamma indicates that most of the diversification occurred early in the history of the clade. According to the inferred phylogeny, the genus Orthopsyche McFarlane is a synonym under Caledopsyche Kimmins, and Abacaria caledona Oláh & Barnard should also be included in Caledopsyche. Main conclusions The age of the radiation does not support a vicariance origin of New Caledonian Hydropsychinae caddisflies. Environmental diversification pre‐dates lineage diversification, and thus environmental heterogeneity potentially played a role in the diversification of the group, by providing a variety of fragmented habitats to disperse into, promoting speciation. The negative gamma indicates that the speciation rate slowed as niches started to fill.     

Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience?

The genus Ceratomyxa (Myxozoa: Myxosporea: Bivalvulida) contains parasites that typically infect the gall bladders of marine teleosts. Species of this genus have also been recorded from elasmobranchs, while the best known species (Ceratomyxa shasta) is a systemic pathogen of fresh water salmonid fishes. Here we characterise 10 new species of Ceratomyxa from marine teleosts using morphometric and rDNA sequence data. A phylogeny of all Ceratomyxa species for which ssrDNA sequence is available was estimated by parsimony, maximum likelihood and Bayesian analyses. Mapping host fish taxonomy, geographic locality and morphology onto the phylogenetic tree provided some concordance of these characters to groups of Ceratomyxa species, but in no case was it consistent throughout the inferred phylogeny. The position of C. shasta as a sister species to the Ceratomyxa clade contradicts previous estimates of marine myxozoan phylogeny which suggested C. shasta was an unrelated lineage. Comparative DNA sequence data is available for more than 17% of some 200 described Ceratomyxa species and the genus now represents one of the most cohesive lineages within the Myxozoa. The independent branching of all atypical Ceratomyxa species and Palliatus indecorus, indicates a review of the diagnostic characters and possible division into more genera is warranted when further data are available.     

The queer Tetraëdron minimum from Lake Kivu (Eastern Africa): is it a result of a human impact?

The coccal unicellular green algal genus Tetraëdron Kütz. ex Korshikov, which can be easily identified by its typical polygonal shape, is a common member of freshwater plankton and metaphyton, frequently observed in lowland temperate and tropical waters. During the analysis of samples from tropical Lake Kivu (Eastern Africa), we found an interesting “lemon-shaped” alga, which, after observations in light microscope and scanning electron microscope, had been listed as Tetraëdron sp. Isolation in pure culture allowed a deeper study on morphology at different stages of the life cycle and the partial sequencing of the 18S rDNA. The results from the different combined approaches confirmed that it belongs to the species Tetraëdron minimum (A. Braun) Hansg. The unusual “lemon-shaped” forms predominant in Lake Kivu are young stages of the life cycle. This study contributes to the knowledge of the morphological variability, reproduction, and resting stages of T. minimum and discusses the reasons for the dominance of such unusual shape found in Lake Kivu, a lake strongly impacted by human activities as resulted by the large-scale biomanipulation following the introduction of the “Tanganyika sardine,” Limnothrissa miodon (Boulenger, 1906), at the end of the 1950s.     

The geography of speciation in narrow‐range endemics of the ‘Haenydra’ lineage (Coleoptera,Hydraenidae, Hydraena)

Aim We test whether species of western Mediterranean aquatic Coleoptera of the ‘Haenydra’ lineage (Hydraenidae, Hydraena) originated through: (1) successive periods of dispersal and speciation, (2) range fragmentation by random vicariance, or (3) range fragmentation by geographic isolation owing to a general reduction of population density. Location Europe. Methods To discriminate between scenarios we use contrasting predictions of the relationship between phylogenetic and geographic distance. The phylogeny was based on 3 kb of four mitochondrial and two nuclear gene fragments of about half of the known species of ‘Haenydra’, including most western Mediterranean taxa. Divergences were estimated using a molecular clock. The relationship between phylogenetic and geographic distance was tested using bivariate plots, Mantel tests and comparison of the observed phylogeny with the one minimizing geographic distances between species, as measured using Euclidean minimum spanning trees (EMSTs). Results The monophyly of ‘Haenydra’ was strongly supported, although its phylogenetic placement was not resolved. ‘Haenydra’ was estimated to be of late Miocene age, with most species originating during the Pleistocene. In two clades (Hydraena tatii and Hydraena emarginata clades) there was a significant association between geographic and phylogenetic distance, and the reconstructed phylogeny was identical to that obtained through the EMST, demonstrating a strong non‐randomness of the geographic distribution of the species. In two other clades (Hydraena iberica and Hydraena bitruncata clades) there was no association between geographic and phylogenetic distance, and the observed phylogeny was not the one minimizing geographic distances. In one of the clades this seems to be due to a secondary, recent range expansion of one species (H. iberica), which erased the geographic signal of their distributions. Main conclusions We show that it is possible to obtain strong evidence of stasis of the geographic ranges of narrow‐range endemic species through the study of their phylogenetic relationships and current distributions. In at least two of the studied clades, current species seem to have originated through the fragmentation of a more widely distributed species, without further range movements. A process of range expansion and fragmentation may have occurred repeatedly within the ‘Haenydra’ lineage, contributing to the accumulation of narrow‐range endemics in Mediterranean Pleistocene refugia.