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.     

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...     

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.     

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.

     

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.     

Molecular analyses of ostracod flocks from Lake Baikal and Lake Tanganyika

Ancient lakes are excellent laboratories for evolutionary research, where species can be studied in the cradle where they originated. In this article, we investigate two endemic ostracod species flocks from the two oldest lakes in the world, Lake Baikal (LB) (ca. 28 myr) and Lake Tanganyika (LT) (ca. 12 myr), with DNA sequence data. Nuclear ITS1 failed to resolve the phylogeny of both flocks. Whilst most phylogenetic relationships of the Tanganyika flock are resolved with mitochondrial COI, the Baikalian tree contains multifurications of up to seven different clades. The Tanganyikan Cyprideis flock shows higher genetic variability, which matches its higher morphological variability. A significant deviation from a constant divergence rate through time indicates that the Cytherissa flock most likely experienced explosive speciation events during its earlier history. Comparative analyses of substitution rates furthermore revealed that they are not clock-wise for COI. Ancestral Cytherissa probably radiated in LB 5–8 myr ago, around the time when the cold, oxygenated abyss was formed in LB. The Tanganyikan Cyprideis flock is almost twice as old as the Baikalian Cytherissa flock, and possibly older than LT itself, ca. 15 myr. The Cyprideis flock has survived drastic lake level changes and resulting salinity crises during its entire history.     

Interspecific relationships of aufwuchs-eating fishes in Lake Tanganyika

Synopsis On a rocky shore of Lake Tanganyika aufwuchs-eating is practiced by 18 fish species: 17 cichlids and 1 cyprinid. The majority takes mostly either filamentous or unicellular algae.Tropheus moorei and its taxonomically related species most closely resemble one another in diet among the species taking mostly filamentous algae, and thePetrochromis species do so among the species taking mostly unicellular algae.Petrochromis polyodon andT. moorei severely interfere with the feeding activities of related species. These two dominant species share both intensive grazing sites and temporal grazing patterns, and there seems to be a symbiotic relationship between them. Symbiotic relationships are also seen in seven cases of associated feeding by carnivorous fishes. Differences in diet or feeding behavior are found between these symbionts. Small but clear differences are found betweenP. polyodon andT. moorei and between the associating and the carnivorous host fishes in the four cases of associated feeding. These small differences seem attributable to morphological differences and may have been effective for the evolution of symbiotic relationships.Contribution from the Laboratory of Animal Ecology, Kyoto University, No. 461.     

Axes of differentiation in the bower-building cichlids of Lake Malawi

The 500-1000 cichlid species endemic to Lake Malawi constitute one of the most rapid and extensive radiations of vertebrates known. There is a growing debate over the role natural and sexual selection have played in creating this remarkable assemblage of species. Phylogenetic analysis of the Lake Malawi species flock has been confounded by the lack of appropriate morphological characters and an exceptional rate of speciation, which has allowed ancestral molecular polymorphisms to persist within species. To overcome this problem we used amplified fragment length polymorphism (AFLP) to reconstruct the evolution of species within three genera of Lake Malawi sand-dwelling cichlids that construct elaborate male display platforms, or bowers. Sister taxa with distinct bower morphologies, and that exist in discrete leks separated by only 1-2 m of depth, are divergent in both sexually selected and ecological traits. Our phylogeny suggests that the forces of sexual and ecological selection are intertwined during the speciation of this group and that specific bower characteristics and trophic morphologies have evolved repeatedly. These results suggest that trophic morphology and bower form may be inappropriate characters for delineating taxonomic lineages. Specifically the morphological characters used to describe the genera Lethrinops and Tramitichromis do not define monophyletic clades. Using a combination of behavioural and genetic characters, we were able to identify several cryptic cichlid species on a single beach, which suggests that sand dweller species richness has been severely underestimated.     

Inheritance pattern of lateral dimorphism in two cichlids (a scale eater, Perissodus microlepis, and an herbivore, Neolamprologus moorii) in Lake Tanganyika

Antisymmetry in the direction of the mouth opening, to either the right ("lefty") or left ("righty"), was documented in the scale-eating cichlid Perissodus microlepis. This study revealed the presence of lefty and righty mouth morphs in the herbivorous cichlid Neolamprologus moorii, although the degree of deviation was not large. Both species are biparental brooders and guard their young. We examined the inheritance pattern of the dimorphism (laterality) using parents and broods of P. microlepis and N. moorii collected in the wild. In P. microlepis, lefty-lefty pairs had a 2:1 frequency of lefty:righty young, lefty-righty pairs a similar number of each type of young, and righty-righty pairs only righty young. Similar inheritance patterns were observed in N. moorii. We propose two hypotheses to explain the inheritance pattern: Mendelian genetics with the lefty allele dominant over the righty and the dominant allele homozygous lethal, and cross-incompatibility that is predominant in lefty homozygotes.     

Plasticity of opsin gene expression in cichlids from Lake Malawi

Sensory systems play crucial roles in survival and reproduction. Therefore, sensory plasticity has important evolutionary implications. In this study, we examined retinal plasticity in five species of cichlid fish from Lake Malawi. We compared the cone opsin expression profiles of wild‐caught fish to lab‐reared F₁ that had been raised in a UV minus, reduced intensity light environment. All of the opsin genes that were expressed in wild‐caught fish were also expressed in lab‐reared individuals. However, we found statistically significant differences in relative opsin expression among all five species. The most consistent difference was in the SWS2B (violet) opsin, which was always expressed at higher levels in lab‐reared individuals. Estimates of visual pigment quantum catch suggest that this change in expression would increase retinal sensitivity in the light environment of the lab. We also found that the magnitude of plasticity varied across species. These findings have important implications for understanding the genetic regulation of opsin expression and raise many interesting questions about how the cichlid visual system develops. They also suggest that sensory plasticity may have facilitated the ecological diversification of cichlids in Lake Malawi.     

Abundance and biomass of heterotrophic microorganisms in Lake Tanganyika

1. This study focused on heterotrophic microorganisms in the two main basins (north and south) of Lake Tanganyika during dry and wet seasons in 2002. Bacteria (81% cocci) were abundant (2.28–5.30 × 10⁶ cells mL^?1). During the dry season, in the south basin, bacterial biomass reached a maximum of 2.27 g C m^?2 and phytoplankton biomass was 3.75 g C m^?2 (integrated over a water column of 100 m). 2. Protozoan abundance was constituted of 99% of heterotrophic nanoflagellates (HNF). Communities of flagellates and bacteria consisted of very small but numerous cells. Flagellates were often the main planktonic compartment, with a biomass of 3.42–4.43 g C m^?2. Flagellate biomass was in the same range and often higher than the total autotrophic biomass (1.60–4.72 g C m^?2). 3. Total autotrophic carbon was partly sustained by the endosymbiotic zoochlorellae Strombidium. These ciliates were present only in the euphotic zone and usually contributed most of the biomass of ciliates. 4. Total heterotrophic ciliate biomass ranged between 0.35 and 0.44 g C m^?2. In 2002, heterotrophic microorganisms consisting of bacteria, flagellates and ciliates represented a large fraction of plankton. These results support the hypothesis that the microbial food web contributes to the high productivity of Lake Tanganyika. 5. As the sole source of carbon in the pelagic zone of this large lake is phytoplankton production, planktonic heterotrophs ultimately depend on autochthonous organic carbon, most probably dissolved organic carbon (DOC) from algal excretion.     

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.     

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.