Functional coupling constrains craniofacial diversification in Lake Tanganyika cichlids

Functional coupling, where a single morphological trait performs multiple functions, is a universal feature of organismal design. Theory suggests that functional coupling may constrain the rate of phenotypic evolution, yet empirical tests of this hypothesis are rare. In fish, the evolutionary transition from guarding the eggs on a sandy/rocky substrate (i.e. substrate guarding) to mouthbrooding introduces a novel function to the craniofacial system and offers an ideal opportunity to test the functional coupling hypothesis. Using a combination of geometric morphometrics and a recently developed phylogenetic comparative method, we found that head morphology evolution was 43% faster in substrate guarding species than in mouthbrooding species. Furthermore, for species in which females were solely responsible for mouthbrooding the males had a higher rate of head morphology evolution than in those with bi-parental mouthbrooding. Our results support the hypothesis that adaptations resulting in functional coupling constrain phenotypic evolution.     

Evolution of brain–body allometry in Lake Tanganyika cichlids

Brain size is strongly associated with body size in all vertebrates. This relationship has been hypothesized to be an important constraint on adaptive brain size evolution. The essential assumption behind this idea is that static (i.e., within species) brain–body allometry has low ability to evolve. However, recent studies have reported mixed support for this view. Here, we examine brain–body static allometry in Lake Tanganyika cichlids using a phylogenetic comparative framework. We found considerable variation in the static allometric intercept, which explained the majority of variation in absolute and relative brain size. In contrast, the slope of the brain–body static allometry had relatively low variation, which explained less variation in absolute and relative brain size compared to the intercept and body size. Further examination of the tempo and mode of evolution of static allometric parameters confirmed these observations. Moreover, the estimated evolutionary parameters indicate that the limited observed variation in the static allometric slope could be a result of strong stabilizing selection. Overall, our findings suggest that the brain–body static allometric slope may represent an evolutionary constraint in Lake Tanganyika cichlids.     

Foraging behaviour and functional morphology of two scale-eating cichlids from Lake Tanganyika

The foraging behaviours of two Tanganyikan scale-eating cichlids, Perissodus straeleni and Perissodus microlepis , were observed in laboratory. Video analyses of their feeding behaviours showed the distinct differences in scale-eating action between the two species. Perissodus straeleni presses and shifts its mouth laterally along the body of the prey as the prey attempts to break free. In contrast, P. microlepis quickly rotates its body, with both jaws pressed tightly against the flank of the prey. Scanning electron microscopy of tooth shapes confirmed that dental morphology clearly differs between the two species: the teeth of P. straeleni are laminar and leaf-shaped with sharp edges along the lateral sides, whereas P. microlepis has thick, broad-based teeth with spine-like points in the upper corners. In addition, inspection of tooth condition in wild-caught fishes showed that the ratio of wearing teeth was significantly higher in P. straeleni than in P. microlepis . These results indicate that the functional morphology of the teeth plays an important role in their scale-eating actions; in P. straeleni , the sharp edges of the teeth appear to function as blades for scraping while shifting the mouth laterally along the body of the prey, whereas the spine-like projections on the teeth of P. microlepis appear to effectively catch scales while pressing and rotating the mouth, simultaneously wrenching off scales. These results clearly demonstrate that the different scale-eating behaviours of the two species are closely associated with the functional diversification of their jaw teeth.     

Ecophysiology of Aufwuchs-eating cichlids in Lake Tanganyika: niche separation by trophic specialization

Synopsis The Aufwuchs-eating cichlids of Lake Tanganyika show clear trophic differences that are correlated to their morphology, physiology and foraging behaviour. The species are grouped into three categories of relative intestinal length according to their feeding habits. A correlation between the intestinal length and the diet could be demonstrated, ranging from around 2.5 for species ingesting more animal food, to 7.8 for detritivorous and microalgivorous species. The relative intestinal length of domesticTropheus moorii, raised in aquaria was significantly lower than that of wild individuals by a factor of 1.7, demonstrating a wide range of phenotypic adaptability. The activities of trypsin and amylase were at an equal level in four Aufwuchseating species, but the activity of laminarinase of a detritivorous-microalgivorous species (Petrochromis orthognathus) was 2.6 times higher than that of an algivorous species (Tropheus moorii). The laminarinase seems to be an excellent marker enzyme for detritivorous or microalgivorous feeding.     

Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika

A recent phylogenetic analysis of mitochondrial DNA sequences from eretmodine cichlids from Lake Tanganyika indicated independent origins of strikingly similar trophic specializations, such as dentition characters. Because genetic lineages with similar trophic morphologies were not monophyletic, but instead were grouped with lineages with different trophic phenotypes, raises the question of whether trophic morphology covaries with additional morphological characters. Here, we quantified morphological variation in body shape and trophically associated traits among eretmodine cichlids using linear measurements, meristic counts and landmark‐based geometric morphometrics. A canonical variates analysis (CVA) delineated groups consistent with dentition characters. Multivariate regression and partial least squares analyses indicated that body shape was significantly associated with trophic morphology. When the phylogenetic relationships among taxa were taken into account using comparative methods, the covariation of body shape and trophic morphology persisted, indicating that phylogenetic relationships were not wholly responsible for the observed pattern. We hypothesize that trophic ecology may be a key factor promoting morphological differentiation, and postulate that similar body shape and feeding structures have evolved multiple times in independent lineages, enabling taxa to invade similar adaptive zones.     

Only true pelagics mix: comparative phylogeography of deepwater bathybatine cichlids from Lake Tanganyika

Hydrobiologia - In the absence of dispersal barriers, species with great dispersal ability are expected to show little, if at all, phylogeographic structure. The East African Great Lakes and their...     

Tactic for bower acquisition by male cichlids,Cyathopharynx furcifer,in Lake Tanganyika

A tactic for bower acquisition by male cichlids,Cyathopharynx furcifer, was studied in Lake Tanganyika. Males held crater-shaped bowers of sand within their territories, which were located adjacent to each other. Females visited bowers to spawn eggs, subsequently brooding the eggs in their mouths. Some individuals held territories without bowers near those of males with bowers. Although only the males with bowers succeeded in reproduction, they were apparently exhausted by bower maintenance and reproduction, and often deserted their bowers. These were soon occupied by males which had held nearby territories without bowers, such males then engaging in reproductive activity. Although the construction of new bowers by males was observed, such was unsuccessful, probably because too much energy was required and/or the optimal space for bowers was limited. Direct aggression by males without bowers against bower-holding males to deprive the bowers was not observed, possibly due to the high costs of such competition. Therefore, waiting for bower desertion by other males may be the best bower acquisition tactic for males without bowers.     

Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids

Parasite diversity and abundance (parasite load) vary greatly among host species. However, the influence of host traits on variation in parasitism remains poorly understood. Comparative studies of parasite load have largely examined measures of parasite species richness and are predominantly based on records obtained from published data. Consequently, little is known about the relationships between host traits and other aspects of parasite load, such as parasite abundance, prevalence and aggregation. Meanwhile, understanding of parasite species richness may be clouded by limitations associated with data collation from multiple independent sources. We conducted a field study of Lake Tanganyika cichlid fishes and their helminth parasites. Using a Bayesian phylogenetic comparative framework, we tested evolutionary associations between five key host traits (body size, gut length, diet breadth, habitat complexity and number of sympatric hosts) predicted to influence parasitism, together with multiple measures of parasite load. We find that the number of host species that a particular host may encounter due to its habitat preferences emerges as a factor of general importance for parasite diversity, abundance and prevalence, but not parasite aggregation. In contrast, body size and gut size are positively related to aspects of parasite load within, but not between species. The influence of host phylogeny varies considerably among measures of parasite load, with the greatest influence exerted on parasite diversity. These results reveal that both host morphology and biotic interactions are key determinants of host–parasite associations and that consideration of multiple aspects of parasite load is required to fully understand patterns in parasitism.     

Reverse evolution in RH1 for adaptation of cichlids to water depth in Lake Tanganyika

Reverse evolution is a widespread phenomenon in biology, but the genetic mechanism for the reversal of a genetic change for adaptation to the ancestral state is not known. Here, we report the first case of complete reverse evolution of two amino acids, serine and alanine, at a single position in RH1 opsin pigment for adaptation to water depth. We determined RH1 sequences of cichlid fishes from four tribes of Lake Tanganyika with different habitat depths. Most of the species were divided into two types: RH1 with 292A for species in shallow water or 292S for species in deep water. Both types were adapted to their ambient light environments as indicated by the absorption spectra of the RH1 pigments. Based on the RH1 locus tree and ecological data, we inferred the ancestral amino acids at position 292 and the distribution of the depth ranges (shallow or deep) of ancestral species of each tribe. According to these estimates, we identified two distinct parallel adaptive evolutions: The replacement A292S occurred at least four times for adaptation from shallow to deep water, and the opposite replacement S292A occurred three times for adaptation from deep to shallow water. The latter parallelism represents the complete reverse evolution from the derived to the ancestral state, following back adaptive mutation with reversal of the RH1 pigment function accompanied by reversal of the species habitat shift.     

A link between host dispersal and parasite diversity in two sympatric cichlids of Lake Tanganyika

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Mating systems of two midwater-spawning cichlids,Cyprichromis microlepidotus andParacyprichromis brieni,in Lake Tanganyika

The breeding habits of 2 maternal mouthbrooding cichlids,Cyprichromis microlepidotus andParacyprichromis brieni, were investigated in Lake Tanganyika. Although spawning on the substrate in the male's mating territory is prevalent in maternal mouthbrooders, bothC. microlepidotus andP. brieni spawned in the water column. MaleC. microlepidotus established their mating territories in the open water column, while maleP. brieni did so around fixed spawning sites near a vertical rock surface. In both species, females visited male mating territories, departing soon after spawning and collecting the eggs. Sneaking, which was observed only inP. brieni, may be attributed to the presence of refuges for sneakers in this species. FemaleC. microlepidotus deposited their entire clutch of about 9 eggs in one male territory. In contrast, femaleP. brieni divided their clutch of about 11 eggs among several males. After the final egg-release, femaleC. microlepidotus repeatedly approached their mate, with the mouth near the abdomen of the latter (nuzzling), but femaleP. brieni often departed without nuzzling. Males may eject sperm during nuzzling to fertilize eggs inside the female's mouth. However, maleP. brieni is also known to eject sperm near spawning females when the females are not nuzzling. Such behavior seems to be a male countermeasure against female mate infidelity, because males could not ensure paternity of eggs by ejecting sperm only during female nuzzling.     

Intestinal coiling pattern in the epilithic algal-feeding cichlids (Pisces, Teleostei) of Lake Tanganyika, and its phylogenetic significance

This paper suggests that, on the basis of ontogenetic change in intestinal coiling pattern, four types and four subtypes could be recognized within 20 species of epilithic algal-feeding cichlids in Lake Tanganyika. The phylogenetically useful anatomical features characterizing each type are as follows. Petrochromis type: torsion of the intestinal tract generally occurs at Stage 5 Intersecting Point (IP), and the haplochromine loop and a two-loop coiling system are observable. Cyathopharynx type: the value of IP becomes 7 before torsion occurs, and the coiling system changes qualitatively from one-loop to two-loop types. Asprotilapia type: torsion occurs at Stage 5 IP, and a one-loop coiling system is retained throughout ontogeny. Telmatochromis type: no torsion occurs, and a one-loop coiling system is retained throughout ontogeny. Within the Petrochromis type, each of the four subtypes is characterized by the following features. Petrochromis subtype: the rostrally directed haplochromine loop has its rostral part situated to the right side of the stomach in the adult stage. Pseudosimochromis subtype: a circular haplochromine loop is present. Eretmodus subtype: the haplochromine loop tends to be prolonged and bends through 90 or 180 further counter-clockwise. Tropheus subtype: torsion occurs at Stage 7 IP.     

Drivers of phytoplankton diversity in Lake Tanganyika

In keeping with the theme of this volume, the present article commemorates the 50 years of Hutchinson’s (Am Nat 93:145–159, 1959) famous publication on the ‘very general question of animal diversity’, which obviously leads to the more important question regarding the driving forces of biodiversity and their limitation in various habitats. The study of phytoplankton in large lakes is a challenging task which requires the use of a wide variety of techniques to capture the range of spatial and temporal variations. The analysis of marker pigments may provide an adequate tool for phytoplankton surveys in large water bodies, thanks to automated analysis for processing numerous individual samples, and by achieving sufficient taxonomic resolution for ecological studies. Chlorophylls and carotenoids were analysed by HPLC in water column samples of Lake Tanganyika from 2002 through 2006, at two study sites, off Kigoma (north basin) and off Mpulungu (south basin). Using the CHEMTAX software for calculating contributions of the main algal groups to chlorophyll a, variations of phytoplankton composition and biomass were determined. We also investigated selected samples according to standard taxonomic techniques for elucidating the dominant species composition. Most of the phytoplankton biomass was located in the 0–40 m layer, with maxima at 0 or 20 m, and more rarely at 40 m. Deep chlorophyll maxima (DCM) and surface ‘blooms’ were occasionally observed. The phytoplankton assemblage was essentially dominated by chlorophytes and cyanobacteria, with diatoms developing mainly in the dry season. The dominant cyanobacteria were very small unicells (mostly Synechococcus), which were much more abundant in the southern basin, whereas green algae dominated on average at the northern site. A canonical correspondence analysis (CCA) including the main limnological variables, dissolved nutrients and zooplankton abundance was run to explore environment–phytoplankton relations. The CCA points to physical factors, site and season as key determinants of the phytoplankton assemblage, but also indicates a significant role, depending on the studied site, of calanoid copepods and of nauplii stages. Our data suggest that the factors allowing coexistence of several phytoplankton taxa in the pelagic zone of Lake Tanganyika are likely differential vertical distribution in the water column, which allows spatial partitioning of light and nutrients, and temporal variability (occurring at time scales preventing long-term dominance by a single taxon), along with effects of predation by grazers.     

Diet disparity among sympatric herbivorous cichlids in the same ecomorphs in Lake Tanganyika: amplicon pyrosequences on algal farms and stomach contents

Background

Lake Tanganyika, an ancient lake in the Great Rift Valley, is famous for the adaptive radiation of cichlids. Five tribes of the Cichlidae family have acquired herbivory, with five ecomorphs: grazers, browsers, scrapers, biters and scoopers. Sixteen species of the herbivorous cichlids coexist on a rocky littoral slope in the lake. Seven of them individually defend feeding territories against intruding herbivores to establish algal farms. We collected epiphyton from these territories at various depths and also gathered fish specimens. Algal and cyanobacteria community structures were analysed using the amplicon-metagenomic method.

Results

Based on 454-pyrosequencing of SSU rRNA gene sequences, we identified 300 phototrophic taxa, including 197 cyanobacteria, 57 bacillariophytes, and 31 chlorophytes. Algal farms differed significantly in their composition among cichlid species, even in the same ecomorph, due in part to their habitat-depth segregation. The algal species composition of the stomach contents and algal farms of each species differed, suggesting that cichlids selectively harvest their farms. The stomach contents were highly diverse, even between species in the same tribe, in the same feeding ecomorph.

Conclusions

In this study, the amplicon-metagenomic approach revealed food niche separation based on habitat-depth segregation among coexisting herbivorous cichlids in the same ecomorphs in Lake Tanganyika.

     

Mitochondrial genome primers for Lake Malawi cichlids

Resolving the evolutionary history of rapidly diversifying lineages like the Lake Malawi Cichlid Flock demands powerful phylogenetic tools. Although this clade of over 500 species of fish likely diversified in less than two million years, the availability of extensive sequence data sets, such as complete mitochondrial genomes, could help resolve evolutionary patterns in this group. Using a large number of newly developed primers, we generated whole mitochondrial genome sequences for 14 Lake Malawi cichlids. We compared sequence divergence across protein‐coding regions of the mitochondrial genome and also compared divergence in the mitochondrial loci to divergence at two nuclear protein‐coding loci, Mitfb and Dlx2. Despite the widespread sharing of haplotypes of identical sequences at individual loci, the combined use of all protein‐coding mitochondrial loci provided a bifurcating phylogenetic hypothesis for the exemplars of major lineages within the Lake Malawi cichlid radiation. The primers presented here could have substantial utility for evolutionary analyses of mitochondrial evolution and hybridization within this diverse clade.     

Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids

The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large-scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.     

Alloparental care between catfishes in Lake Tanganyika

A bagrid catfish Auchenoglanis occidentalis cared for its brood, deposited within an accumulation of shells and gravel in the centre of a large saucer-like depression, for up to 2 weeks in Lake Tanganyika. Adults of another catfish Dinotopterus cunningtoni (Clariidae) persistently came to A. occidentalis nests near days of host spawning. Eggs of D. cunningtoni were found in the host nests on the day and within 2 days of host spawning. During and for a few days after the end of host brooding, associate species' young of much older ages than the host brood were often found in the nests together with those of a similar age to the host young. Associate young were rarely found in nests before spawning and in unused nests. These findings suggested that this brood-mixing has two origins: egg dumping by associate adults and voluntary intrusion of large associate young into host nests. Possible benefits to the associate species are to take advantage of nest preparation and parental behaviour of the host species and to feed on the host brood.     

Paternal mouthbrooding bagrid catfishes in Lake Tanganyika

 This article gives the first information about paternal mouthbrooding in bagrid catfishes, based on analysis of specimens collected while SCUBA diving in Lake Tanganyika, Africa. Lophiobagrus aquilus and L. cyclurus, endemic to the lake, were nocturnally active, and in the daytime were found concealed singly or in pairs beneath rocks. Among 39 L. aquilus and 52 L. cyclurus collected, 8 and 1 solitary males, respectively, were incubating eggs or young in the buccal cavity. Paired males and females and solitary females never took care of the offspring. In both species, females of pairs showed much higher gonadosomatic index values and had larger oocytes in the ovaries than did solitary females. This fact suggests that pair formation takes place at a time near the gonadal maturation of the female and that the pair separate after spawning. We tentatively propose an evolutionary transition route of care patterns in bagrid catfishes. Received: January 25, 2002 / Revised: April 13, 2002 / Accepted: April 17, 2002     

Evolution of a unique predatory feeding apparatus: functional anatomy,development and a genetic locus for jaw laterality in Lake Tanganyika scale-eating cichlids

Background  

While bilaterality is a defining characteristic of triploblastic animals, several assemblages have managed to break this symmetry in order to exploit the adaptive peaks garnered through the lateralization of behaviour or morphology. One striking example of an evolved asymmetry in vertebrates comes from a group of scale-eating cichlid fishes from Lake Tanganyika. Members of the Perissodini tribe of cichlid fishes have evolved dental and craniofacial asymmetries in order to more effectively remove scales from the left or right flanks of prey. Here we examine the evolution and development of craniofacial morphology and laterality among Lake Tanganyika scale-eating cichlids.