Explosive speciation in cichlid fishes of the African Great Lakes: a dynamic model of adaptive radiation

In the African cichlid species flocks several corresponding ecotypes and species communities have evolved independently in each of the lakes. These flocks can be viewed as reiterations of a process, induced by the same type of external event (the formation of a lake) and seeded by the same group of organisms, equipped with the same innovative potential. The East African lakes differ in their ages, so that different stages of adaptive radiation of a single group of fishes can be studied simultaneously. This review combines findings on various African cichlid species flocks and derives a generalized model of cichlid adaptive radiation. The model constitutes four stages, defined by the most influential habitat characteristics and interactions among members of the species community at each phase. It is an attempt to provide an explicit hypothesis for a dynamic evolutionary process, as a basis to future studies.     

Food resources of shrimp-eating cichlid fishes in Lake Tanganyika

Species, size composition, and diurnal variation in abundance of shrimp (Atyidae) were examined and compared with food habits of 14 species of shrimp-eating cichlids in Lake Tanganyika. In the daytime when the cichlids foraged actively, only one species of shrimp, Limnocaridina latipes, was present on rock surfaces. Eleven of the 14 species of shrimp-eaters examined preyed mainly on L. latipes; the shrimp-eaters foraging only on rock surfaces preyed exclusively on L. latipes, whereas shrimp-eaters also taking foods from the interstices between or under stones and debris preyed on various species of shrimp. Although three kinds of shrimp-eaters, each with a unique prey catching technique and preferred shrimp size, were recognized, all shrimp-eaters preyed on shrimp of greatly overlapping sizes. This fact confirms that partitioning of food resources takes place via different capturing techniques. Moreover, the utilization of the same food resource in a different manner may promote group foraging in some shrimp-eaters, because the shrimp is a suitable animal to hunt in groups and is a quickly renewable food of potential abundance.     

Dichromatism in relation to the trophic biology of predatory cichlid fishes in Lake Tanganyika, East Africa

A population of the piscivorous Tanganyikan cichlid, Lepidiolamprologus profundicola contains individually distinct pale and dark colour morphs: a dichromatism not related to age or sex. The 'dark form' frequently targets prey from the shaded space under rocks, while the 'plae form' targets prey in well-iluminated open water. This hunting site specialization is not ascribable to the differences of microhabitat that the predators of each form encounter. The main function of the dichromatism is apparently cryptic, as a camouflage for hunting. Interspecific comparisons among 19 species of carnivorous Tanganyikan cichlid fishes reveal that dichromatic taxa generally chase an active prey: fishes, scales of fishes or highly mobile free-swimming crustacea. In contrast, cichlid species foraging on a sessile or sluggish prey are monochromatic. This finding strongly supports the hypothesis that a pale-dark dichromatism serves to optimize foraging efficiency in predatory cichlids hunting an active prey.     

Trophic interrelationships amongst cichlid fishes in a tropical African reservoir (Lake Chivero,Zimbabwe)

The diet of seven cichlid species of Lake Chivero, Zimbabwe, was investigated from October 2004 to April 2005 to determine the degree of dietary overlap and interspecific competition. These fish could be separated into four groups. Two microphages, Oreochromis niloticus and O. macrochir, fed mostly on blue-green algae and their diets, in all size classes, overlapped almost completely. This suggested a high degree of competition between the two species and may account for the fact that O. niloticus, introduced into the lake in the 1980s is now the dominant species. There was also a significant dietary overlap between the two macrophages Tilapia sparrmanii and T. rendalli, which were macrophages with macrophytes as a significant component of their diet. Interspecific competition between these two species may account for the increase in the abundance of T. sparrmanii and a decrease in the numbers of T. rendalli over the last two decades. The diet of two small omnivores Pharyngochromis acuticeps and Pseudocrenilabrus philander consisted of algae, zooplankton, plant material, fish and detritus and also overlapped extensively, but these species probably avoid competition by living in different habitats; P. philander is usually associated with vegetation while P. acuticeps tends to live in more open waters. The last species, Serranochromis robustus, was largely piscivorous. There were no ontogenetic variations in diet, apart from P. acuticeps where small fish fed mainly on zooplankton becoming omnivorous in larger ones, and S. robustus where the diet shifted from zooplankton in specimens <50 mm SL to fish in larger size classes. Data available from the 1960s and 1970s indicate that the diets of some species have changed with invertebrates such as chironomid larvae being previously more important in all diets, while most species now take a higher proportion of algae. This reflects changes in the lake, which is eutrophic and has experienced severe algal blooms since 1960. Handling editor: C. Strumbauer     

Food habits and foraging behaviour of benthivorous cichlid fishes in Lake Tanganyika

Synopsis A study was made of the food habits and foraging behaviour of coexisting benthivorous cichlid fishes along the rocky northwestern coast of Lake Tanganyika. The five group-foraging species regularly found in the study area,Gnathochromis pfefferi, Lamprologus callipterus, Altolamprologus compressiceps, Lepidiolamprologus elongatus andLobochilotes labiatus, have different foraging techniques, although all eat shrimps (family Atyidae). Individuals of each species allow potential food-competitors to forage within its foraging area, increasing its own chances of finding shrimps disturbed by the foraging action of such competitors. In these five shrimp-eating species, group foraging thus occurs in a mutualistic context. A super-abundance of shrimps may allow the coexistence of shrimp-eaters with different foraging techniques, and furthermore, their coexistence itself may promote cooperative group-foraging among them. Three benthivorous cichlids,Neolamprologus mondabu, N. tretocephalus andN. leleupi, were indifferent to, or excluded, the group foraging species because these three individual-foraging species exploit different food items or employ similar foraging techniques to the group-foraging species.     

Phylogenetic study of cichlid fishes in Lake Tanganyika: a lepidological approach

The phylogeny of the various cichlid lineages in Lake Tanganyika has been investigated applying scale morphology and squamation characters. The monophyly of the established tribes is assessed and evidence is given for their interrelationships as well as their phyletic position within the family Cichlidae.     

Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas

Lake Tanganyika, the oldest of the East African Great Lakes, harbors the ecologically, morphologically, and behaviorally most complex of all assemblages of cichlid fishes, consisting of about 200 described species. The evolutionary old age of the cichlid assemblage, its extreme degree of morphological differentiation, the lack of species with intermediate morphologies, and the rapidity of lineage formation have made evolutionary reconstruction difficult. The number and origin of seeding lineages, particularly the possible contribution of riverine haplochromine cichlids to endemic lacustrine lineages, remains unclear. Our phylogenetic analyses, based on mitochondrial DNA sequences of three gene segments of 49 species (25% of all described species, up to 2,400 bp each), yield robust phylogenies that provide new insights into the Lake Tanganyika adaptive radiation as well as into the origin of the Central- and East-African haplochromine faunas. Our data suggest that eight ancient African lineages may have seeded the Tanganyikan cichlid radiation. One of these seeding lineages, probably comprising substrate spawning Lamprologus-like species, diversified into six lineages that evolved mouthbrooding during the initial stage of the radiation. All analyzed haplochromines from surrounding rivers and lakes seem to have evolved within the radiating Tanganyikan lineages. Thus, our findings contradict the current hypothesis that ancestral riverine haplochromines colonized Lake Tanganyika to give rise to at least part of its spectacular endemic cichlid species assemblage. Instead, the early phases of the Tanganyikan radiation affected Central and East African rivers and lakes. The haplochromines may have evolved in the Tanganyikan basin before the lake became a hydrologically and ecologically closed system and then secondarily colonized surrounding rivers. Apparently, therefore, the current diversity of Central and East African haplochromines represents a relatively young and polyphyletic fauna that evolved from or in parallel to lineages now endemic to Lake Tanganyika.     

Geographical colour variation in cichlid fishes at the southern end of Lake Tanganyika

Synopsis Geographical colour variation and distribution of 48 common cichlid fish species were studied at 20 sites along an 85 km shoreline at the southern end of Lake Tanganyika, Africa. Sixteen species had two or more colour morphs and 11 species showed a limited distribution in the study area. They were all rock-dwellers. Distributional borders of the color morphs and species with a limited distribution mostly lay in two long sandy beaches, 7 and 13 km long. We suggest that the long sandy beaches can be effective barriers against dispersal of shallow-water rock-dwelling cichlid fishes.     

Lunar synchronization of spawning in cichlid fishes of the tribe Lamprologini in Lake Tanganyika

Lunar synchronization of spawning was investigated for eight substrate brooding cichlid fishes belonging to the tribe Lamprologini. Their spawning activities all peaked during the second quarter of the lunar cycle. Comparison between their breeding styles and the degrees of spawning synchronization suggested that the nocturnal guarding-efficiency of eggs, especially exposed ones, is improved by the maximal amount of moonlight during full moon and, in species whose young leave the breeding sites about 2 weeks after spawning, the survival of dispersing young is enhanced by the darkness of moonless nights.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Mitochondrial phylogeny of the Cyprichromini, a lineage of open-water cichlid fishes endemic to Lake Tanganyika, East Africa

We present a phylogeny of the Cyprichromini, a lineage of cichlid fishes from Lake Tanganyika, showing progressive adaptation towards pelagic life style. Our study is based upon three mitochondrial gene segments, 443 bp of the control region, 402 bp of the cytochrome b gene and the entire NADH dehydrogenase subunit 2 gene (1047 bp). The topologies obtained by different tree building methods subdivide the Cyprichromini into four distinct lineages: the Paracyprichromis-, the Cyprichromis zonatus-, the Cyprichromis microlepidotus-lineage, and a lineage comprising Cyprichromis pavo and Cyprichromis leptosoma. Our study thus corroborates the distinctness of C. zonatus which was recently described formally. Concerning ecology and mating behavior, a clear evolutionary trend towards progressive adaptation to the pelagic zone emerges during the evolution of the Cyprichromini. The linearized tree analysis further shows that the four lineages have split almost contemporaneously. The mean Kimura-2-parameter distance among the four lineages emerging from the primary radiation of the Cyprichromini amounts to 7.21% and is in close agreement to that previously found for the primary radiation of the tribe Tropheini (7.01%), a lineage of rock-dwelling cichlids endemic to Lake Tanganyika. To date, the influence of lake level fluctuations as promoters of diversification has been demonstrated only for rock-dwelling cichlids. Based on the agreement in temporary patterns of diversification, we suggest that Pleistocene lake level changes have left a similar genetic imprint in a group of cichlid fishes that progressively colonized the open water during their radiation.     

Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation

Antarctic notothenioid fishes represent a rare example of a marine species flock. They evolved special adaptations to the extreme environment of the Southern Ocean including antifreeze glycoproteins. Although lacking a swim bladder, notothenioids have diversified from their benthic ancestor into a wide array of water column niches, such as epibenthic, semipelagic, cryopelagic and pelagic habitats. Applying stable carbon (C) and nitrogen (N) isotope analyses to gain information on feeding ecology and foraging habitats, we tested whether ecological diversification along the benthic–pelagic axis followed a single directional trend in notothenioids, or whether it evolved independently in several lineages. Population samples of 25 different notothenioid species were collected around the Antarctic Peninsula, the South Orkneys and the South Sandwich Islands. The C and N stable isotope signatures span a broad range (mean δ¹³C and δ¹⁵N values between ?25.4‰ and ?21.9‰ and between 8.5‰ and 13.8‰, respectively), and pairwise niche overlap between four notothenioid families was highly significant. Analysis of isotopic disparity‐through‐time on the basis of Bayesian inference and maximum‐likelihood phylogenies, performed on a concatenated mitochondrial (cyt b) and nuclear gene (myh6, Ptr and tbr1) data set (3148 bp), showed that ecological diversification into overlapping feeding niches has occurred multiple times in parallel in different notothenioid families. This convergent diversification in habitat and trophic ecology is a sign of interspecific competition and characteristic for adaptive radiations.     

Overshooting dynamics in a model adaptive radiation

The history of life is punctuated by repeated periods of unusually rapid evolutionary diversification called adaptive radiation. The dynamics of diversity during a radiation reflect an overshooting pattern with an initial phase of exponential-like increase followed by a slower decline. Much attention has been paid to the factors that drive the increase phase, but far less is known about the causes of the decline phase. Decreases in diversity are rarely associated with climatic changes or catastrophic events, suggesting that they may be an intrinsic consequence of diversification. We experimentally identify the factors responsible for losses in diversity during the later stages of the model adaptive radiation of the bacterium Pseudomonas fluorescens. Proximately, diversity declines because of the loss of biofilm-forming niche specialist morphotypes. We show that this loss occurs despite the presence of strong divergent selection late in the radiation and is associated with continued adaptation of resident niche specialists to both the biotic and abiotic environments. These results suggest that losses of diversity in the latter stages of an adaptive radiation may be a general consequence of diversification through competition and lends support to the idea that the conditions favouring the emergence of diversity are different from those that ensure its long-term maintenance.     

Mitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes from Lake Tanganyika in eastern Africa

Of the three cichlid species flocks in eastern Africa, Lake Tanganyika harbors the oldest species assemblage, which is also the most diverse morphologically and behaviorally. For 12 species (20 individuals) of 12 genera of the tribe Ectodini, 852 bp from two segments (cytochrome b and control region) of the mitochondrial genome were sequenced. In addition, orthologous sequences were obtained from eight species (11 individuals) representing other mouthbrooding lineages from Lake Tanganyika. Comparisons of sequence divergences revealed that the single Tanganyikan tribe Ectodini appears to be approximately five times older than the whole Lake Malawi cichlid species flock, suggesting that the radiation of the Tanganyikan mouthbrooding lineages took place long before the species flocks of Lakes Malawi and Victoria evolved. Seven of nine surveyed tribes of Tanganyikan cichlids appear to be approximately equally divergent, and this seems to corroborate the hypothesis of a rapid simultaneous formation of lineages at an early stage in the history of the Lake Tanganyika species flock. The close genetic relationship between the endemic Tropheus lineage and a nonendemic "Haplochromine," Astatotilapia burtoni, indicates that members of the tribe Tropheini may be the sister group of the cichlid flocks of Lakes Malawi and Victoria. The phylogenetic analyses demonstrate the monophyly of the Ectodini and identify the Cyprichromini as their sister group among the Tanganyikan cichlids. Within the tribe Ectodini the molecular data suggest both a branching pattern different than that previously proposed and a subdivision of the Ectodini into four clades, instead of the two originally described. The previously postulated model of morphological transformations believed to be responsible for the drastically different types of ecological specialization found among the Ectodini might therefore be in need of reinterpretation. Characters immediately related to foraging and nutrition seem to be particularly prone to homoplasy, even among members of a single lineage of cichlid fishes.      

Gene duplications and the evolution of c-type lysozyme during adaptive radiation of East African cichlid fish

Given the reported degraded nature of DOC in the Rio Negro, and low oxygen, pH, and bacterial riverine levels, we hypothesized: (1) DOC would have strong humic and fulvic acid fluorescence signals with high aromaticity and large mean molecular weight; and (2) photo-oxidation rates would be slow, and reactive oxygen species (ROS) concentrations low, producing no oxidative stress in biota. We surveyed the environment and properties of DOC and explored DOC photo-oxidation and fish sensitivity to DOC products. DOC properties were investigated using absorption and fluorescence indices and parallel factor analysis (PARAFAC) of excitation–emission matrices. ROS concentrations were measured spectrophotometrically. A native fish, Hemigrammus levis, was exposed to photo-oxidizing DOC and its tissues (brain, gill, liver) assayed for changes in antioxidant and biotransformation enzymes. With respect to our hypotheses, (1) DOC was highly terrigenous, with high SAC₃₄₀ values (aromaticity), high capacity to produce ROS, and high tryptophan-like fluorescence (bacterial, autochthonous signal); (2) photo-oxidation rates were appreciable, while products were related to mean UV-radiation levels (total radiation was constant). ROS levels were often higher than freshwater averages, yet fish experienced no oxidative stress. Results suggest photo-oxidation influences patterns in C-cycling, bacterial production and community dynamics between wet and dry seasons.     

Evolutionary history of the endemic Lake Tanganyika cichlid fish Tylochromis polylepis: a recent intruder to a mature adaptive radiation

With an age of 9–12 million years (Myr) Lake Tanganyika holds the oldest and most complex species flock of cichlid fishes. It is believed to be of polyphyletic origin and rooted in nine ancient African lineages, six of which underwent diversification, while three remained monotypic. Here, the evolutionary history, route and timing of colonization were analyzed, as well as intraspecific genetic diversity of Tylochromis polylepis , the single albeit endemic representative of the tribe Tylochromini in Lake Tanganyika. The role of Tylochromis in the radiation was uncertain and the species was suggested to be either an ancient colonizer or a recent addition to the fauna. With 2.8–4.2% sequence divergence to four congeners living in Lakes Bangweulu and Mweru (Upper Congo River) as well as from Luozi River and Lake Etsotso (Lower Congo River), the species appears to be a recent colonizer, which is likely to have diverged from its riverine allies less than 510 000 years ago. The ability to enter an adaptive radiation at a highly mature stage with its densely packed species community and fine-tuned niche segregation seems remarkable. So far it was assumed that all Tanganyikan endemics evolved within the lake ecosystem by intralacustrine speciation, and that complex competitive interactions among endemics tighten the system against intruders. The intruding species can be classified as a generalist living over muddy bottom in the lake and in river estuaries. Microgeographic substructuring is suggested, possibly because of geographic segregation of breeding sites. Concerning the route of colonization, a downstream movement via one of the inflowing rivers situated in the south of Lake Tanganyika is suggested.     

Intraspecific brood-mixing of the cichlid fishPerissodus microlepis in Lake Tanganyika

Synopsis The frequency and origin of intraspecific brood-mixing in the biparental cichlid fishPerissodus microlepis were investigated by the cohort analysis of schooling young and the underwater observation of guarding parents. The cohort analysis showed that brood-mixing started from the early guarding state when the young were smaller than 10 mm standard length and nearly all schools of young larger than 16 mm contained alien young from up to 6 broods. Brood farming-out of this fish, which was originally proposed to be a way adopted only by a deserted parent, was performed also by paired parents. We suggest that brood-mixing inP. microlepis is attributed mainly to brood farming-out by paired and deserted parents.     

Phylogeographic history of the genus Tropheus,a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika

Lake Tanganyika contains the oldest and most complex flock of cichlid fishes counting about 200 endemic species. It is comprised of 16 ecologically, morphologically and genetically highly distinct tribes. Many species are further subdivided into arrays of geographic morphs, each colonizing particular sections of the shore line. The genus Tropheus represents the most spectacular and best studied example for this phenomenon, counting more than 100 distinctly colored populations and sister species, some living in sympatry. Their present distribution and genetic structure was shaped by a series of lake level fluctuations which caused cycles of isolation and secondary admixis. The present study extends previous work on the phylogeography of Tropheus and aims at the fine-scale reconstruction of the origin and spread of lineages in the central and southern basin of the lake. The previously defined mtDNA lineages were evaluated on the basis of statistical parsimony networks. Haplotype networks were created for each lineage and related to their centers of diversity in terms of present distribution. A linearized tree analysis and a mismatch distribution analysis corroborate two of the three radiation waves suggested in earlier works, but the new data suggest a different primary colonization scenario for the southern basin.