Role of thyroid hormone in the ontogeny and morphological diversification of <Emphasis Type="Italic">Barbus intermedius sensu</Emphasis> Banister, 1973 of Lake Tana in Ethiopia

The role of thyroid hormone in the ontogeny of the Large African barb Barbus intermedius sensu Banister, 1973 (Teleostei; Cyprinidae)—the presumed ancestral species for the species flock of the large African Barbs of Lake Tana (Ethiopia)—has been studied. It has been shown that the thyroid hormone influences the timing and rate of many morphogenetic processes and a change in its level causes heterochronies, affecting the definitive morphology of fish. Thus, it can be assumed that even a slight change in activity of the thyroid axis during ontogeny can be the cause of wide morphological variability in B. intermedius and may underlie explosive diversification of the species flock of Large African Barbs of Lake Tana.     

Observations on reproduction of the Lake Tana barbs

During the rainy season (September–November 1994), in tributaries of Lake Tana (Ethiopia), the Gumara, Gelda and Negashu, barbs of diVerent morphotypes were ready to spawn, running and spent. The most numerous were barbs similar to Barbus intermedius common in many rivers of the Ethiopian Highlands. They were also found spawning in the Gumara and Gelda Rivers in the dry season (February 1996, 1997). There were no evident diVerences in time and place of spawning of barbs representing diVerent morphotypes. Only zurki, bigmouth mini-eye and bighead were not found in the rivers. Spatial and temporal segregation may contribute to reproductive isolation of morphotypes spawning in rivers, but if reproductive isolation exists the main role must be played by diVerences in mating behaviour. Morphotypes of the Lake Tana barbs have diVerent migration patterns. Barbs similar to the riverine B. intermedius may spend their lives in rivers or in the lake, moving to and fro. Barbs of acute, bigmouth big-eye and, perhaps, other morphotypes migrate downstream as alevins or fry, stay in the lake for several years and migrate back into rivers for spawning after reaching maturity.     

Spawning migrations of the endemic Labeobarbus (Cyprinidae, Teleostei) species of Lake Tana, Ethiopia: status and threats

The reproductive biology of the only known intact species flock of large cyprinids, the 16 Labeobarbus species of Lake Tana (Ethiopia), has been extensively studied for the past two decades. Seven species of Labeobarbus are known to migrate >50 km upstream into tributary rivers for spawning during the rainy season (July to October), whereas eight other species are absent from these rivers and probably developed a new strategy of lacustrine spawning (macro-spatial segregation). One species (L. intermedius) probably spawns in the lake as well as in the rivers. Between the early 1990s and 2000s, the riverine spawners showed a decline of 75% in both biomass and number in both fishery independent surveys and in commercial catches. Reproductive migration makes fishes vulnerable to fisheries and other threats like habitat modifications. Lacustrine spawners are probably more resilient as they are not known to form spawning aggregations that can easily be exploited by fishermen. In addition, upstream rivers and catchments around Lake Tana are highly degraded by erosion and recently subjected to intensive habitat modification for irrigation and hydroelectric power generation. This article reviews results of field studies on the Labeobarbus spawning migration from Lake Tana to spawning rivers, giving emphasis on segregation and homing. It also summarizes existing and emerging threats which form potential causes for the decline of the migratory Labeobarbus species. Knowledge gaps on the reproductive biology are identified for further investigation.     

Major histocompatibility genes in the Lake Tana African large barb species flock: evidence for complete partitioning of class II B, but not class I, genes among different species

The 16 African large barb fish species of Lake Tana inhabit different ecological niches, exploit different food webs and have different temporal and spatial spawning patterns within the lake. This unique fish species flock is thought to be the result of adaptive radiation within the past 5 million years. Previous analyses of major histocompatibility class II B exon 2 sequences in four Lake Tana African large barb species revealed that these sequences are indeed under selection. No sharing of class II B alleles was observed among the four Lake Tana African large barb species. In this study we analysed the class II B exon 2 sequences of seven additional Lake Tana African large barb species and African large barbs from the Blue Nile and its tributaries. In addition, the presence and variability of major histocompatibility complex class I UA exon 3 sequences in six Lake Tana and Blue Nile African large barb species was analysed. Phylogenetic lineages are maintained by purifying or neutral selection on non-peptide binding regions. Class II B intron 1 and exon 2 sequences were not shared among the different Lake Tana African large barb species or with the riverine barb species. In contrast, identical class I UA exon 3 sequences were found both in the lacustrine and riverine barb species. Our analyses demonstrate complete partitioning of class II B alleles among Lake Tana African large barb species. In contrast, class I alleles remain for the large part shared among species. These different modes of evolution probably reflect the unlinked nature of major histocompatibility genes in teleost fishes.Electronic Supplementary Material Supplementary material is available for this article at .An erratum to this article can be found at     

Genetic divergence among morphotypes of Lake Tana (Ethiopia) barbs

The genus Barbus is a paraphyletic assemblage that includes three different ploidy levels: diploid, tetraploid and hexaploid. 'B.' intermedins , which inhabits Lake Tana (Ethiopia), is a hexaploid taxon that forms a 'species flock' consisting of at least 14 morphotypes. Thirty-one presumptive allozymic loci were analysed in a large sample of 'B.' intermedius. No diagnostic loci were observed between the morphotypes, but substantial differences in allele frequencies were found. One morphotype, Acute, differs significantly from the others. The presence of this genetic differentiation within the lake strongly suggests that the morphotypes are diverging lineages. Because of some parallel characteristics with cichlid species flocks, we put forward the hypothesis that the morphotypes of barbs in Lake Tana represent a species flock that originated via sympatric speciation with more rapid morphological than molecular differentiation. If the differentiation and the reproductive isolation are real, it is probable that the morphotypes already are or will soon reach the status of species.     

Lake Tana large barbs diversity: Developmental and hormonal bases

Helerochronies caused by changes in the hormonal status are proposed to play a major role in the diversification of the Lake Tana barbs of Labeobarbus (=Barbus) genus (Dgebuadze and Mina, 2008). To test this hypothesis, we (i) compared temporal patterns of cranial development in L. intermedius, likely ancestral for Tana species flock, and L. brevicephalus and L. megastoma proposed to be paedomoiphic and peramoiphic, respectively; (ii) studied the role of thyroid hormone (TH) in the regulation of L. intermedius development; (iii) evaluated the effect of TH changes on the definitive morphology, and (iv) evaluated the possible role of TH in diversification of Tana barbs. Skull development was found to be heterochronicaily changed in L. brevicephalus and L. megastoma as compared to L. intermedius; revealed heteroclironies may account for differences in skull proportions distinguishing these barbs, TH was shown to play a major role in the regulation of ontogeny. Changes in TH level cause heterochronies in the development of a skull, axial skeleton, fins and fin girdles, squamation, and dentition. Heteroclironies were shown to influence adult morphology of these structures. These findings support the hypothesis of the involvement of developmental and hormonal factors in the diversification of the Lake Tana large barbs.     

The Bathyclarias-Clarias species flock. A new model to understand rapid speciation in African great lakes

Phylogenetic relationships between seven species of the catfish species flock from Lake Malawi (genus Bathyclarias) and other Clariid catfish have been investigated using cytochrome b partial sequences. Here we demonstrate that this species flock originated from a widespread, generalist species, Clarias gariepinus, still occurring in the lake. Bathyclarias species and their ancestor C. gariepinus form a simple model that can be used to understand the mechanisms of adaptation and rapid speciation in African Great lakes.     

Spawning of large <Emphasis Type="Italic">Barbus</Emphasis> (<Emphasis Type="Italic">Barbus intermedins</Emphasis> Complex) in a small river of the Lake Tana basin (Ethiopia) and relationships of some putative species

Direct observations on three forms (morph types) of spawning barbs, considered by some authors as different species, were carried out in September–October 2005 at the Gumara River and its small tributary, the Ducalit, in the Lake Tana basin. The spawning barbs were sampled using cast nets. Barbs of different morphotypes composed common spawning aggregations and were caught together. It is likely that troutlike females mate extensively with intermedius males and, probably, with bigmouth small-eye males. Experiments in artificial fertilization and rearing showed that, during the embryonic period, there was no increase in mortality of progeny from crosses of barbs of different morphotypes, in comparison with homonomic crosses, thus suggesting an absence of postzygotic reproductive isolation between the morphotypes. At the same time, mortality of progeny from crossing barbs with Varicorhinus beso Rüppell, 1836 was very high during the earliest stages of development, suggesting strong, even if incomplete, reproductive isolation ensured by postzygotic mechanisms. Published in Voprosy Ikhtiologii, 2007, Vol. 47, No. 5, pp. 676–683. The article was translated by the authors.     

Toothless predators: feeding performance and techniques among the piscivores within Lake Tana's endemic barbus species flock (Pisces:Cyprinidae)

With more than 2000 fish species the Cyprinidae is the largest family of vertebrates. Lake Tana, a large lake (3050 km²) situated in the NW‐ highlands of Ethiopia, harbours, as far as we know the only remaining intact species flock of large (max. 100 cm FL) cyprinid fishes (15 Barbus spp.). One of the most intriguing aspects of this endemic Barbus species flock is the large number of piscivores (8). Cyprinid fishes seem not well designed for piscivory, they lack teeth in the oral jaw, have a small slit‐shaped pharyngeal cavity and all lack a stomach with low pH for digesting large prey. Many barbs are benthivorous species, like the ancestral barb in Lake Tana's isolated system. Why then is piscivory, which is rare among cyprinids, so common in Lake Tana Barbus? The aim of present study was to compare the performance and techniques of these piscivorous Barbus with known piscivores from other fish families. We studied prey handling times over prey size, prey capture using high‐speed movies, and assessed the effect of prey size on performance and prey selection in the field. Performances were explained by functional morphology of their feeding system. Overall, Lake Tana's piscivorous Barbus perform relatively 'poor', compared to piscivores from other fish families. For example, Lake Tana's piscivores are only able to handle prey fish smaller than 16% of their own body length. However, Lake Tana lacks potential piscivorous competitors, rendering the piscivorous Barbus by far the 'best' and apparently highly successful. They have adapted to all available macro‐habitats (littoral, offshore pelagic and offshore benthic), using different techniques (ambush, pursuit and cruising), a unique scenario for barbs.     

Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach

A unique species flock of large barbs (Barbus spp.) from Lake Tana is presented, from the level of fish stocks to molecules. Evidence is given for the species status of 14 morphotypes of large barbs. They distinctly differ in: (1) head and body morphometrics, (2) food preferences, (3) distribution patterns, (4) maximal body size, (5) spawning area and period, and (6) molecular genetic characters. Most types show early morphological divergence at small size. Major Histocompatibility Complex (MHC) genes, encoding cell membrane proteins involved in defence against pathogens, were found to be diagnostic for the species' genetic identity. A strong selective pressure on particular amino acid positions in the MHC protein sequence most probably arose in response to different pathogen loads from the newly invaded ecological niches after formation of Lake Tana, ca. two million years ago.Arguments for a sympatric origin of this species flock are discussed. An evolutionary scenario suggests a riverine ancestral Barbus intermedius invading Lake Tana after its formation by volcanic blocking of the Blue Nile river and its isolation by waterfalls. Specialisation for particular food types and disruptive selection on many feeding structures are hypothesized as the evolutionary drive in speciation. The causal relationship between the diversity in feeding structures and food types is explained from experiments and models. As an example, the potential food niche of three barb species is predicted from parameter values measured from a large set of feeding structures and tested against the actual gut contents. The co-occurrence of eight piscivorous barb species is unique for cyprinid fish, which lack oral jaw teeth and a stomach. The significance of this aquatic ecosystem as a multidisciplinary evolutionary laboratory and the need for a wise balance between exploitation and conservation is stressed.     

Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock

Phylogenetic analyses based on mitochondrial (mt) DNA have indicated that the cichlid species flock of the Lake Victoria region is derived from a single ancestral species found in East African rivers, closely related to the ancestor of the Lake Malawi cichlid species flock. The Lake Victoria flock contains ten times less mtDNA variation than the Lake Malawi radiation, consistent with current estimates of the ages of the lakes. We present results of a phylogenetic investigation using nuclear (amplified fragment length polymorphism) markers and a wider coverage of riverine haplochromines. We demonstrate that the Lake Victoria-Edward flock is derived from the morphologically and ecologically diverse cichlid genus Thoracochromis from the Congo and Nile, rather than from the phenotypically conservative East African Astatotilapia. This implies that the ability to express much of the morphological diversity found in the species flock may by far pre-date the origin of the flock. Our data indicate that the nuclear diversity of the Lake Victoria-Edward species flock is similar to that of the Lake Malawi flock, indicating that the genetic diversity is considerably older than the 15 000 years that have passed since the lake began to refill. Most of this variation is manifested in trans-species polymorphisms, indicating very recent cladogenesis from a genetically very diverse founder stock. Our data do not confirm strict monophyly of either of the species flocks, but raise the possibility that these flocks have arisen from hybrid swarms.     

Phenetic relationships and probable ways of morphological diversification of the African large barbs (<Emphasis Type="Italic">Barbus intermedius</Emphasis> complex) in Lake Tana (Ethiopia)

29 quantitative and 18 qualitative skull characters were studied in the African large barbs (Barbus intermedius complex) from Lake Tana (Ethiopia). Based on results of principle components analysis phenetic relationships of 12 morphotypes were assessed. External features diagnostic of the morphotypes were found in individuals substantially different in the skull characters. The obtained data along with the data on morphological diversity of large barbs from Ethiopia beyond the Lake Tana basin suggest origination of the Lake Tana complex of forms from a complex of forms that existed in the upper reaches of the Blue Nile before the lake came into being, and the extant morphotypes of the Lake Tana barbs originated from three or four forms that composed the ancestral riverine local complex.     

Rapid evolution of an ancient lake species flock: Freshwater limpets (Gastropoda: Ancylidae) in the Balkan Lake Ohrid

Ancient lakes have long been recognized as evolutionary theatres and hot spots of endemism; the evolution of their morphologically often highly diverse species flocks has received much attention. However, as each ancient lake has its own geological and evolutionary history, modes of speciation may differ from system to system. Ancient lakes can act as evolutionary reservoirs that assure the survival of relict species, but at the same time extant species may evolve through intralacustrine speciation. Other aspects of interest are the actual rates of immigration, diversification or extinction as well as the temporal framework of morphological change. Many of these questions have been addressed in the African (e.g. Lake Tanganyika) and Asian (e.g. Lake Baikal) ancient lakes. For an European ancient lakes (e.g. Lakes Ohrid and Prespa), such studies are largely missing. In the present paper, extraordinarily shaped endemic freshwater limpets of the genus Ancylus from the Balkan Lake Ohrid are used in a phylogeographic and phylogenetic context to test whether they represent an ancient lake species flock, to study the mode of speciation, and to assess the timing of morphological change. Based on DNA data from two mitochondrial genes (COI, LSU rDNA), it has been found that the Lake Ohrid Ancylus species form an endemic monophyletic group. In addition, the lake's feeder springs are inhabited by another, undescribed Ancylus species. All other studied waterbodies within the watershed do not support their own Ancylus lineages but are inhabited by a widespread Mediterranean taxon. The split between the species endemic to the lake and its sister taxon is dated to 1.4±0.6 million years ago. The study presents the first genetic confirmation for the existence of a species flock in a European ancient lake. Contrary to the prevailing opinion it shows that, concerning Ancylus, Lake Ohrid represents a site of intralacustrine speciation rather than an evolutionary reservoir. Moreover, it provides the first evidence for rapid morphological change in an European ancient lake species flock. See also Electronic Supplement at: http://www.senckenberg.de/odes/06-12.htm.     

Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids.

Allopatric processes of speciation have routinely been presented to explain the extraordinary radiation of the East African Great Lakes cichlid fish species flocks. The 21 or more species of pelagic cichlids within the Lake Malawi flock appear to have lake-wide distributions that challenge such a concept. Data from six microsatellite DNA loci indicate single, panmictic populations across the lake of three Diplotaxodon species. Levels of variability at these loci suggest that populations have been large and stable. Mitochondrial DNA sequence data (872 bp of control region + 981 bp of the NADH-2) from 90 species, representing all major clades within the Lake Malawi flock, indicate reciprocal monophyly of the pelagic clade. We suggest that these data support a hypothesis that speciation in sympatry is more plausible (and widespread) within the cichlid species flocks than previously thought.     

Impact of rifting and hydrography on the genetic structure of Clarias gariepinus in eastern Africa

In a study of the genetic structure of Clarias gariepinus at the ND5 and ND6 loci of mitochondrial DNA using RFLP–PCR in 16 populations (267 fish), a total of 18 haplotypes was detected. The most common haplotype was EA1 and represented 46% of all genotypes. Three phylogenetic groups characterized the region, with the East African clade occurring between the western rift in the west, Lake Baringo in the north, the Indian Ocean in the east and the Rufiji River in the south. The Lower Tana River (unlike the Upper Tana River) and Lake Kamnarok grouped with the North clade, while the Ruaha River (tributary of the Rufiji River) represented a contact zone between the East and the South-central African clade. Genetic structure was distinct ( F _ST=0·66), with the Lower Tana River and Lake Mtera forming specific units. Within the East clade, the Oloibortoto River, Upper Tana River and Lake Victoria each formed a distinct population. Lake Baringo grouped either with the eastern rift or the western rift depending on the analysis. Lake Jipe, the Pangani River, Rusizi River, Lake Edward, Nyabugogo River and the Luiche River clustered together. Among group variance explained 66·8% of the total variance; the impact of vicariance (rifting and uplifting) on the phylogeography was considerable. A distribution model of the catfish is proposed which combines the separation by rifting several million years ago with a high gene flow in the western rift due to historical connectivity among lakes and rivers.     

Phylogenetic Relationships Among East African Haplochromine Fish as Revealed by Short Interspersed Elements (SINEs)

Genomic DNA libraries were prepared from two endemic species of Lake Victoria haplochromine (cichlid) fish and used to isolate and characterize a set of short interspersed elements (SINEs). The distribution and sequences of the SINEs were used to infer phylogenetic relationships among East African haplochromines. The SINE-based classification divides the fish into four groups, which, in order of their divergence from a stem lineage, are the endemic Lake Tanganyika flock (group 1); fish of the nonendemic, monotypic, widely distributed genus Astatoreochromis (group 2); the endemic Lake Malawi flock (group 3); and group 4, which contains fish from widely dispersed East African localities including Lakes Victoria, Edward, George, Albert, and Rukwa, as well as many rivers. The group 4 haplochromines are characterized by a subset of polymorphic SINEs, each of which is present in some individuals and absent in others of the same population at a given locality, the same morphologically defined species, and the same mtDNA-defined haplogroup. SINE-defined group 4 contains six of the seven previously described mtDNA haplogroups. One of the polymorphic SINEs appears to be fixed in the endemic Lake Victoria flock; four others display the presence-or-absence polymorphism within the species of this flock. These findings have implications for the origin of Lake Victoria cichlids and for their founding population sizes.     

Evolution of the ribosomal RNA internal transcribed spacer one (ITS-1) in cichlid fishes of the Lake Victoria region

The nucleotide sequences of the first internal transcribed spacer (ITS-1) of the ribosomal RNA gene cluster have been determined for 11 species of closely related endemic cichlid fishes of the Lake Victoria region (LVR) and 6 related East African cichlids. The ITS-1 sequences confirmed independently derived basal phylogenies, but provide limited insight within this species flock. The line leading to Pseudocrenilabrus multicolor arose early, close to the divergence event that separated the tilapiine and haplochromine tribes of the "African Group" of the family Cichlidae. In this phylogeny, Astatoreochromis alluaudi and the riverine Astatotilapia burtoni are sister taxa, which together are a sister group to a monophyletic assemblage including both Lake Victoria and Lake Edward taxa. The ITS-1 data support the monophyly of haplochromine genera across lakes. Since Lake Victoria is believed to have been dry between 14, 500 and 12,400 BPE, the modern assemblage must have been derived from reinvasion by the products of earlier cladogenesis events. Thus, although the regional superflock is monophyletic, the haplochromines of Lake Victoria itself did not evolve in situ from a single ancestor.     

On the origin of the Synodontis catfish species flock from Lake Tanganyika

Species flocks within Great Lakes provide unique insights into the factors affecting diversification. Lake Tanganyika (LT) is of particular interest because it contains many endemic groups for which general factors affecting diversification can be discerned. Here, we present the first phylogenetic study of the LT Synodontis (Siluriformes, Mochokidae) species flock using mtDNA sequence data. Our data reveal some previously unrecognized species diversity and indicate that the LT species flock is not monophyletic, and that two closely related clades of endemics may have independently colonized LT. Other comparable small species flocks are characterized by a single colonization event. Molecular date estimates of the timing of the initial within-lake diversification of the LT endemics, based on a fossil calibration, are comparable to those reported for other groups, suggesting that extrinsic factors maybe important common causes of clade diversification. The basal divergence in the sampled Synodontis reveals an East-West African faunal split seen in many terrestrial, but few aquatic groups, the timing of which coincides with East African rifting events.     

Lacustrine radiations in African Synodontis catfish

Synodontis catfish are a species‐rich, tropical pan‐African genus that predominately occur in fluviatile environments, but which also form a small radiation within Lake Tanganyika (LT). Here we estimate Synodontis relationships, based on mitochondrial and nuclear DNA, greatly expanding previous sampling. Data were analysed using different methods of phylogenetic inference: Bayesian (also testing compositional heterogeneity), likelihood and parsimony, in order to investigate biogeographic history and the extent of intralacustrine speciation within this group. Bayesian‐relaxed clock analyses were used to estimate timings of radiations. Our analyses reveal a single origin of the LT flock with the inclusion of the nonendemic S. victoriae, and that these taxa evolved relatively recently (5.5 Ma), considerably later than the formation of LT (9–12 Ma). Two internal endemic clades diversified at a similar time (2–2.5 Ma), corresponding to a period of climate change, when lake levels dropped. We find evidence for a further species flock, composed of riverine southern African taxa, the diversification of which is very rapid, 0.8 Ma (95% HPD: 0.4–1.5) and infer a similar scenario for the diversification of this flock to southern African serrachromine cichlids in that they radiated in the now extinct lake Makgadikgadi. We also reveal that the biogeographic history of Synodontis catfish is more complex than previously thought, with nonmonophyletic geographic species groupings.