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Behavioral lateralization has been documented in many vertebrates. The scale-eating cichlid fish Perissodus microlepis is well known for exhibiting lateral dimorphism in its mouth morphology and lateralized behavior in robbing scales from prey fish. A previous field study indicated that this mouth asymmetry closely correlates with the side on which prey is attacked, but details of this species' predation behavior have not been previously analyzed because of the rapidity of the movements. Here, we studied scale-eating behavior in cichlids in a tank through high-speed video monitoring and quantitative assessment of behavioral laterality and kinematics. The fish observed showed a clear bias toward striking on one side, which closely correlated with their asymmetric mouth morphologies. Furthermore, the maximum angular velocity and amplitude of body flexion were significantly larger during attacks on the preferred side compared to those on the nonpreferred side, permitting increased predation success. In contrast, no such lateral difference in movement elements was observed in acoustically evoked flexion during the escape response, which is similar to flexion during scale eating and suggests that they share a common motor control pathway. Thus the neuronal circuits controlling body flexion during scale eating may be functionally lateralized upstream of this common motor pathway.

Lake Tanganyika is the oldest of the Great Ancient Lakes in the East Africa. This lake harbours about 250 species of cichlid fish, which are highly diverse in terms of morphology, behaviour, and ecology. Lake Tanganyika's cichlid diversity has evolved through explosive speciation and is treated as a textbook example of adaptive radiation, the rapid differentiation of a single ancestor into an array of species that differ in traits used to exploit their environments and resources. To elucidate the processes and mechanisms underlying the rapid speciation and adaptive radiation of Lake Tanganyika's cichlid species assemblage it is important to integrate evidence from several lines of research. Great efforts have been, are, and certainly will be taken to solve the mystery of how so many cichlid species evolved in so little time. In the present review, we summarize morphological studies that relate to the adaptive radiation of Lake Tanganyika's cichlids and highlight their importance for understanding the process of adaptive radiation.

The factors promoting the evolution of parental care strategies have been extensively studied in experiment and theory. However, most attempts to examine parental care in an evolutionary context have evaluated broad taxonomic categories. The explosive and recent diversifications of East African cichlid fishes offer exceptional opportunities to study the evolution of various life history traits based on species-level phylogenies. The Xenotilapia lineage within the endemic Lake Tanganyika cichlid tribe Ectodini comprises species that display either biparental or maternal only brood care and hence offers a unique opportunity to study the evolution of distinct parental care strategies in a phylogenetic framework. In order to reconstruct the evolutionary relationships among 16 species of this lineage we scored 2,478 Amplified Fragment Length Polymorphisms (AFLPs) across the genome. We find that the Ectodini genus Enantiopus is embedded within the genus Xenotilapia and that during 2.5 to 3 million years of evolution within the Xenotilapia clade there have been 3–5 transitions from maternal only to biparental care. While most previous models suggest that uniparental care (maternal or paternal) arose from biparental care, we conclude from our species-level analysis that the evolution of parental care strategies is not only remarkably fast, but much more labile than previously expected.

Background

Cichlid fishes in Lake Tanganyika exhibit remarkable diversity in their feeding habits. Among them, seven species in the genus Perissodus are known for their unique feeding habit of scale eating with specialized feeding morphology and behaviour. Although the origin of the scale-eating habit has long been questioned, its evolutionary process is still unknown. In the present study, we conducted interspecific phylogenetic analyses for all nine known species in the tribe Perissodini (seven Perissodus and two Haplotaxodon species) using amplified fragment length polymorphism (AFLP) analyses of the nuclear DNA. On the basis of the resultant phylogenetic frameworks, the evolution of their feeding habits was traced using data from analyses of stomach contents, habitat depths, and observations of oral jaw tooth morphology.

Results

AFLP analyses resolved the phylogenetic relationships of the Perissodini, strongly supporting monophyly for each species. The character reconstruction of feeding ecology based on the AFLP tree suggested that scale eating evolved from general carnivorous feeding to highly specialized scale eating. Furthermore, scale eating is suggested to have evolved in deepwater habitats in the lake. Oral jaw tooth shape was also estimated to have diverged in step with specialization for scale eating.

Conclusion

The present evolutionary analyses of feeding ecology and morphology based on the obtained phylogenetic tree demonstrate for the first time the evolutionary process leading from generalised to highly specialized scale eating, with diversification in feeding morphology and behaviour among species.

Supported by evidence for assortative mating and polygynandry, sexual selection through mate choice was suggested as the main force driving the evolution of colour diversity of haplochromine cichlids in Lakes Malawi and Victoria. The phylogenetically closely related tribe Tropheini of Lake Tanganyika includes the genus Tropheus, which comprises over 100 colour variants currently classified into six morphologically similar, polyphyletic species. To assess the potential for sexual selection in this sexually monochromatic maternal mouthbrooder, we used microsatellite-based paternity inference to investigate the mating system of Tropheus moorii. In contrast to haplochromines in Lake Malawi, multiple paternity is rare or even absent in broods of T. moorii. Eighteen of the 19 analysed families were consistent with genetic monogamy, while either a mutation or more than one sire explained the genotype of one offspring in another brood. We discuss the differences in breeding behaviour between T. moorii and the Lake Malawi haplochromines, and evaluate additional factors or alternatives to sexual selection as promoters of colour diversification. A preliminary survey of other Tropheini species suggested that multiple paternity is infrequent in the entire tribe.

Although the cichlid fishes from Lake Tanganyika are treated as a textbook example of adaptive radiation, many taxonomic problems remain unresolved. Cyathopharynx furcifer, which belongs to the currently monospecific genus Cyathopharynx, contains two colour morphs at the southern end of the lake: one has a yellow anal fin, and the other has a black anal fin. Some books for hobbyists of ornamental fish treat these morphs as different species, but taxonomic studies have neither mentioned the existence nor addressed the status of these colour morphs. In the present paper, we analysed these two colour morphs using mitochondrial, microsatellite, morphometric, and meristic data sets. Both molecular and morphological data allowed clear discrimination between these morphs, suggesting the existence of two distinct sympatric species. Three taxonomic species have been described in this genus, and only C. furcifer is currently considered valid. Observations of type specimens of these three nominal species will be needed to determine the scientific names of these colour morphs.

Background

The tribe Lamprologini is the major substrate breeding lineage of Lake Tanganyika's cichlid species flock. Among several different life history strategies found in lamprologines, the adaptation to live and breed in empty gastropod shells is probably the most peculiar. Although shell-breeding arose several times in the evolutionary history of the lamprologines, all obligatory and most facultative shell-breeders belong to the so called "ossified group", a monophyletic lineage within the lamprologine cichlids. Since their distinctive life style enables these species to live and breed in closest vicinity, we hypothesized that these cichlids might be particularly prone to accidental hybridization, and that introgression might have affected the evolutionary history of this cichlid lineage.

Results

Our analyses revealed discrepancies between phylogenetic hypotheses based on mitochondrial and nuclear (AFLP) data. While the nuclear phylogeny was congruent with morphological, behavioral and ecological characteristics, several species – usually highly specialized shell-breeders – were placed at contradicting positions in the mitochondrial phylogeny. The discordant phylogenies strongly suggest repeated incidents of introgressive hybridization between several distantly related shell-breeding species, which reticulated the phylogeny of this group of cichlids. Long interior branches and high bootstrap support for many interior nodes in the mitochondrial phylogeny argue against a major effect of ancient incomplete lineage sorting on the phylogenetic reconstruction. Moreover, we provide morphological and genetic (mtDNA and microsatellites) evidence for ongoing hybridization among distantly related shell-breeders. In these cases, the territorial males of the inferred paternal species are too large to enter the shells of their mate, such that they have to release their sperm over the entrance of the shell to fertilize the eggs. With sperm dispersal by water currents and wave action, trans-specific fertilization of clutches in neighboring shells seem inevitable, when post-zygotic isolation is incomplete.

Conclusion

From the direct observation of hybrids we conclude that hybridization between distantly related gastropod-shell-breeding cichlids of Lake Tanganyika follows inevitably from their ecological specialization. Moreover, the observed incongruence between mtDNA and nuclear multilocus phylogeny suggests that repeated hybridization events among quite distantly related taxa affected the diversification of this group, and introduced reticulation into their phylogeny.

Lake Tanganyika comprises a cichlid species flock with substrate-breeding and mouthbrooding lineages. While sexual selection via mate choice on male mating color is thought to boost speciation rates in mouthbrooding cichlids, this is not the case in substrate-breeding lamprologines, which mostly form stable pairs and lack sexual dichromatism. We present a comprehensive reconstruction of the evolution of the cichlid tribe Lamprologini, based upon mtDNA sequences and multilocus nuclear DNA (AFLP) markers. Twelve mtDNA clades were identified, seven of which were corroborated by the AFLP tree. The radiation is likely to have started about 5.3 MYA, contemporarily with that of the mouthbrooding C-lineage, and probably triggered by the onset of deep-water conditions in Lake Tanganyika. Neither the Congo- nor the Malagarazi River species form the most ancestral branch. Several conflicts in the mtDNA phylogeny with taxonomic assignments based upon color, eco-morphology and behavior could be resolved and complemented by the AFLP analysis. Introgressive hybridization upon secondary contact seems to be the most likely cause for paraphyly of taxa due to mtDNA capture in species involving brood-care helpers, while accidental hybridization best explains the para- or polyphyly of several gastropod shell breeders. Taxonomic error or paraphyly due to the survival of ancestral lineages appear responsible for inconsistencies in the genera Lamprologus and Neolamprologus.

Background

Adaptation to different ecological environments is thought to drive ecological speciation. This phenomenon culminates in the radiations of cichlid fishes in the African Great Lakes. Multiple characteristic traits of cichlids, targeted by natural or sexual selection, are considered among the driving factors of these radiations. Parasites and pathogens have been suggested to initiate or accelerate speciation by triggering both natural and sexual selection. Three prerequisites for parasite-driven speciation can be inferred from ecological speciation theory. The first prerequisite is that different populations experience divergent infection levels. The second prerequisite is that these infection levels cause divergent selection and facilitate adaptive divergence. The third prerequisite is that parasite-driven adaptive divergence facilitates the evolution of reproductive isolation. Here we investigate the first and the second prerequisite in allopatric chromatically differentiated lineages of the rock-dwelling cichlid Tropheus spp. from southern Lake Tanganyika (Central Africa). Macroparasite communities were screened in eight populations belonging to five different colour morphs.

Results

Parasite communities were mainly composed of acanthocephalans, nematodes, monogeneans, copepods, branchiurans, and digeneans. In two consecutive years (2011 and 2012), we observed significant variation across populations for infection with acanthocephalans, nematodes, monogeneans of the genera Gyrodactylus and Cichlidogyrus, and the copepod Ergasilus spp. Overall, parasite community composition differed significantly between populations of different colour morphs. Differences in parasite community composition were stable in time. The genetic structure of Tropheus populations was strong and showed a significant isolation-by-distance pattern, confirming that spatial isolation is limiting host dispersal. Correlations between parasite community composition and Tropheus genetic differentiation were not significant, suggesting that host dispersal does not influence parasite community diversification.

Conclusions

Subject to alternating episodes of isolation and secondary contact because of lake level fluctuations, Tropheus colour morphs are believed to accumulate and maintain genetic differentiation through a combination of vicariance, philopatric behaviour and mate discrimination. Provided that the observed contrasts in parasitism facilitate adaptive divergence among populations in allopatry (which is the current situation), and promote the evolution of reproductive isolation during episodes of sympatry, parasites might facilitate speciation in this genus.

Hybridization among littoral cichlid species in Lake Tanganyika was inferred in several molecular phylogenetic studies. The phenomenon is generally attributed to the lake level-induced shoreline and habitat changes. These allow for allopatric divergence of geographically fragmented populations alternating with locally restricted secondary contact and introgression between incompletely isolated taxa. In contrast, the deepwater habitat is characterized by weak geographic structure and a high potential for gene flow, which may explain the lower species richness of deepwater than littoral lineages. For the same reason, divergent deepwater lineages should have evolved strong intrinsic reproductive isolation already in the incipient stages of diversification, and, consequently, hybridization among established lineages should have been less frequent than in littoral lineages. We test this hypothesis in the endemic Lake Tanganyika deepwater cichlid tribe Bathybatini by comparing phylogenetic trees of Hemibates and Bathybates species obtained with nuclear multilocus AFLP data with a phylogeny based on mitochondrial sequences. Consistent with our hypothesis, largely congruent tree topologies and negative tests for introgression provided no evidence for introgressive hybridization between the deepwater taxa. Together, the nuclear and mitochondrial data established a well-supported phylogeny and suggested ecological segregation during speciation.

The species flocks of cichlid fishes in the East African Lakes Tanganyika, Malawi and Victoria are prime examples of adaptive radiation and explosive speciation. Several hundreds of endemic species have evolved in each of the lakes over the past several thousands to a few millions years. Sexual selection via colour-assortative mating has often been proposed as a probable causal factor for initiating and maintaining reproductive isolation. Here, we report the consequences of human-mediated admixis among differentially coloured populations of the endemic cichlid fish Tropheus moorii from several localities that have accidentally been put in sympatry in a small harbour bay in the very south of Lake Tanganyika. We analysed the phenotypes (coloration) and genotypes (mitochondrial control region and five microsatellite loci) of almost 500 individuals, sampled over 3 consecutive years. Maximum-likelihood-based parenthood analyses and Bayesian inference of population structure revealed that significantly more juveniles are the product of within-colour-morph matings than could be expected under the assumption of random mating. Our results clearly indicate a marked degree of assortative mating with respect to the different colour morphs. Therefore, we postulate that sexual selection based on social interactions and female mate choice has played an important role in the formation and maintenance of the different colour morphs in Tropheus, and is probably common in other maternally mouthbrooding cichlids as well.

Cichlid fishes of Lake Tanganyika display a variety of mating and parental care behaviors, including polygamous and monogamous mouthbrooding and substrate breeding, cooperative breeding, as well as various alternative reproductive tactics such as sneaking and piracy. Moreover, reproductive behaviors sometimes vary within species both in space and in time. Here, I survey reports on mating and parenting behaviors of Lake Tanganyika cichlid species and address the evolution of mating and parental care patterns and sexual dimorphism. Notes on measures of sexual selection intensity and the difficulties of defining mating systems and estimating selection intensities at species level conclude the essay.

Background

Cichlid fishes are notorious for their wealth of intra- and interspecific colour pattern diversity. In Lake Tanganyika, the endemic genus Tropheus represents the most impressive example for geographic variation in the pattern and hue of integument colouration, but the taxonomy of the over 100 mostly allopatric colour morphs remains to a large degree unresolved. Previous studies of mitochondrial DNA sequence data revealed polyphyly of the six nominally described species and complex phylogeographic patterns influenced by lake level fluctuations and population admixture, and suggested the parallel evolution of similar colour patterns in divergent evolutionary lineages. A gene tree of a rapidly radiating group may be subject to incomplete and stochastic lineage sorting, and to overcome this problem we used multi-locus, nuclear AFLP data in comparison with mtDNA sequences to study diversification, migration and introgression in Tropheus colour morphs in Lake Tanganyika.

Results

Significant incongruence between phylogenetic reconstructions from mitochondrial and AFLP data suggested incomplete sorting of mitochondrial haplotypes as well as frequent introgression between differentiated lineages. In contrast to the mitochondrial phylogeny, the AFLP phenogram was largely congruent with species classifications, colour pattern similarities, and in many cases also with the current geographic distribution of populations, and did not produce evidence of convergent colour pattern evolution. Homoplasy in the AFLP data was used to identify populations that were strongly affected by introgression.

Conclusion

Different evolutionary processes were distinguished by the combination of mitochondrial and AFLP data. Mitochondrial phylogeographic patterns retained signals of large-scale migration events triggered by historical, major lake level fluctuations, whereas AFLP data indicated genetic cohesion among local groups of populations resulting from secondary contact of adjacent populations in the course of the more frequently occurring, minor lake level fluctuations. There was no support for the parallel evolution of similar colour patterns in the AFLP data. Genetic signatures of introgression and hybridisation detected in several populations suggest that lake level fluctuations drove the stunning diversification of Tropheus morphs not only through population fragmentation, but also by promoting hybridisation between differentiated morphs in secondary contact.

Ancient lakes are often collectively viewed as evolutionary hot spots of diversification. East Africa's Lake Tanganyika has long been the subject of scientific interest owing to dramatic levels of endemism in species as diverse as cichlid fishes, paludomid gastropods, decapod and ostracod crustaceans and poriferans. It is the largest and deepest of the African rift lakes, and its endemic fauna has been presented with a stable inland environment for over 10 Myr, offering unique opportunities for within-lake diversification. Although astonishing diversification has been documented in the endemic cichlid fauna of the lake, similar patterns of rapid diversification have long been assumed for other groups. In contrast to this hypothesis of rapid speciation, we show here that there has been no acceleration in the rate of speciation in the thalassoid gastropods of the lake following lake colonization. While limited within-lake speciation has occurred, the dramatic conchological diversity of gastropods presently found within the lake has evolved from at least four major lineages that pre-date its formation by as much as 40 Myr. At the same time, a widespread group of African gastropods appears to have evolved from taxa presently found in the lake. While Lake Tanganyika has been a cradle of speciation for cichlid fishes, it has also been an important evolutionary reservoir of gastropod lineages that have been extirpated outside the basin.

Background

The adaptive radiations of cichlid fishes in East Africa are well known for their spectacular diversity and their astonishingly fast rates of speciation. About 80% of all 2,500 cichlid species in East Africa, and virtually all cichlid species from Lakes Victoria (~500 species) and Malawi (~1,000 species) are haplochromines. Here, we present the most extensive phylogenetic and phylogeographic analysis so far that includes about 100 species and is based on about 2,000 bp of the mitochondrial DNA.

Results

Our analyses revealed that all haplochromine lineages are ultimately derived from Lake Tanganyika endemics. We find that the three most ancestral lineages of the haplochromines sensu lato are relatively species poor, albeit widely distributed in Africa, whereas a fourth newly defined lineage – the 'modern haplochromines' – contains an unparalleled diversity that makes up more than 7% of the worlds' ~25,000 teleost species. The modern haplochromines' ancestor, most likely a riverine generalist, repeatedly gave rise to similar ecomorphs now found in several of the species flocks. Also, the Tanganyikan Tropheini are derived from that riverine ancestor suggesting that they successfully re-colonized Lake Tanganyika and speciated in parallel to an already established cichlid adaptive radiation. In contrast to most other known examples of adaptive radiations, these generalist ancestors were derived from highly diverse and specialized endemics from Lake Tanganyika. A reconstruction of life-history traits revealed that in an ancestral lineage leading to the modern haplochromines the characteristic egg-spots on anal fins of male individuals evolved.

Conclusion

We conclude that Lake Tanganyika is the geographic and genetic cradle of all haplochromine lineages. In the ancestors of the replicate adaptive radiations of the 'modern haplochromines', behavioral (maternal mouthbrooding), morphological (egg-spots) and sexually selected (color polymorphism) key-innovations arose. These might be – together with the ecological opportunity that the habitat diversity of the large lakes provides – responsible for their evolutionary success and their propensity for explosive speciation.

Alternative reproductive tactics (ARTs) are found in several Lake Tanganyika shell-brooding cichlids. Field studies were conducted in the Wonzye population to examine reproductive ecology and ARTs in the Lake Tanganyika shell-brooding cichlid Neolamprologus brevis. We discovered that this fish occurred in both rocky- and sandy-bottom habitats, but in rocky habitats, brood-caring females exclusively occurred in shell-patches that another cichlid species created. All N. brevis of both sexes in the patches were sexually mature, whereas immature males and females with unripe eggs were found frequently in sandy-bottom habitats. Males in sandy-bottom habitats were smaller, but fed more frequently and were in better somatic condition than males in the patches. Similar tendency was found in females. This indicates that N. brevis uses different habitats depending on the stage of its life history, with migration from sandy-bottom habitats to the shell-patches for reproduction. Males in the patches exhibited different behavior patterns: floating above the patches and lying in the patches. The former was larger, more aggressive, and invested less in gonads (relative to body size) than the latter. These results accord with those of other shell-brooding Lake Tanganyika cichlids with ARTs, and they therefore suggest the presence of ARTs in N. brevis.

Background

Understanding the causes of disparities in species diversity across taxonomic groups and regions is a fundamental aim in evolutionary biology. Addressing these questions is difficult because of the need for densely sampled phylogenies and suitable empirical systems.

Methodology/Principal Findings

Here we investigate the cichlid fish radiation of Lake Tanganyika and show that per lineage diversification rates have been more than six times slower than in the species flocks of Lakes Victoria and Malawi. The result holds even at peak periods of diversification in Lake Tanganyika, ruling out the age of the lake as an explanation for slow average rates, and is robust to uncertainties over the calibration of cichlid radiations in geological time. Moreover, Lake Tanganyika lineages, irrespective of different biological characteristics (e.g. sexually dichromatic versus sexually monochromatic clades), have diversified at similar rates, falling within typical estimates across a range of plant and animal clades. For example, the mostly sexually dichromatic haplochromines, which have speciated explosively in Lakes Victoria and Malawi, have displayed modest rates in Lake Tanganyika (where they are called Tropheini).

Conclusion/Significance

Our results show that either the Lake Tanganyika environment is less conducive for cichlid speciation or the remarkable diversifying abilities of the haplochromines were inhibited by the prior occupancy of older radiations. Although the results indicate a dominant role for the environment in shaping cichlid diversification, differences in the timing of diversification among the Tanganyikan tribes indicate that biological differences were still important for the dynamics of species build-up in the lake. While we cannot resolve the timing of the radiation relative to the origin of the lake, because of the lack of robust geological date calibrations for cichlids, our results are consistent with a scenario that the different clades reflect independent adaptive radiations into different broad niches in the lake.

This study investigated fine-scale population substructuring in an apparently monogamous, biparental mouth-brooding cichlid. Microsatellite allele frequencies were determined at four polymorphic loci for nine populations of Eretmodus cyanostictus. We provide empirical support for the hypothesis that a species employing this breeding strategy should exhibit high levels of population substructuring. Stretches of sand represent considerable barriers to dispersal and, in contrast to the rock-dwelling cichlids of Lake Malawi, distance alone, along a continuous rocky shoreline, is sufficient to reduce gene flow significantly There was a significant pattern of isolation by distance both along the whole study area and over the stretch of continuous shoreline, suggesting that this species has poor dispersal capabilities and that juveniles establish territories close to their natal site. Despite limited dispersal, E. cyanostictus populations are not significantly more inbred than a more-widely dispersing rock-dwelling cichlid from Lake Malawi. This finding may cast doubt on the hypothesis that polyandry has evolved as a mechanism for maintaining genetic diversity in Lake Malawi cichlids. High levels of substructuring may not always promote high levels of speciation, and other factors, such as the intensity of sexual selection, may be more important in determining the speciation potential of a lineage.

Background

Lake Tanganyika (LT) is the oldest of the African Rift Lakes and is one of the richest freshwater ecosystems on Earth, with high levels of faunal diversity and endemism. The endemic species flocks that occur in this lake, such as cichlid fishes, gastropods, catfish and crabs, provide unique comparative systems for the study of patterns and processes of speciation. Mastacembelid eels (Teleostei: Mastacembelidae) are a predominately riverine family of freshwater fish, occurring across Africa and Asia, but which also form a small species flock in LT.

Methods

Including 25 species across Africa, plus Asian representatives as outgroups, we present the first molecular phylogenetic analysis for the group, focusing particularly on the evolutionary history and biodiversity of LT mastacembelid eels. A combined matrix of nuclear and mitochondrial genes based on 3118 bp are analysed implementing different phylogenetic methods, including Bayesian inference and maximum likelihood.

Results

LT Mastacembelus are recovered as monophyletic, and analyses reveal the rapid diversification of five main LT lineages. Relaxed molecular clock dates provide age estimates for the LT flock at ~7-8 Myr, indicating intralacustrine diversification, with further speciation events coinciding with periods of lower lake level. Our analyses also reveal as yet undescribed diversity of lacustrine and riverine species. A Southern-Eastern African clade, that is younger than the LT flock, is also recovered, while West African taxa are basal members of the African mastacembelid clade.

Conclusions

That the LT species flock of mastacembelid eels appears to have colonised and immediately diversified soon after the formation of the lake, supports the view of LT as an evolutionary hotspot of diversification. We find evidence for biogeographic clades mirroring a similar pattern to other ichthyological faunas. In addition, our analyses also highlight a split of African and Asian mastacembelid eels at ~19 Myr that is considerably younger than the split between their associated continents, suggesting a dispersal scenario for their current distribution.

Scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika display handed (lateralized) foraging behavior, where an asymmetric ‘left’ mouth morph preferentially feeds on the scales of the right side of its victim fish and a ‘right’ morph bites the scales of the left side. This species has therefore become a textbook example of the astonishing degree of ecological specialization and negative frequency-dependent selection. We investigated the strength of handedness of foraging behavior as well as its interaction with morphological mouth laterality in P. microlepis. In wild-caught adult fish we found that mouth laterality is, as expected, a strong predictor of their preferred attack orientation. Also laboratory-reared juvenile fish exhibited a strong laterality in behavioral preference to feed on scales, even at an early age, although the initial level of mouth asymmetry appeared to be small. This suggests that pronounced mouth asymmetry is not a prerequisite for handed foraging behavior in juvenile scale-eating cichlid fish and might suggest that behavioral preference to attack a particular side of the prey plays a role in facilitating morphological asymmetry of this species.

Background

With about 120 colour morphs currently assigned to six nominal species, the genus Tropheus is an ideal model to study evolutionary divergence of populations in allopatry. The morphology of Tropheus has been described as relatively static, but reproductive constraints are sexually dimorphic due to mouthbrooding in females. We analysed phenotypic variation in six populations of T. moorii and one population of T. polli using geometric morphometrics to assess morphological differences among sexes in relation to the differentiation of populations and species.

Results

The mean shapes differed significantly between sexes, populations, and species even though within-sex variation exceeded the divergence among populations. The first principal component of Procrustes shape coordinates revealed differences between populations and species in mouth position and ventral head shape. The second principal component reflected sex-specific shape differences, mainly comprising a relatively larger female viscerocranium and, in particular, a larger buccal area. While shape variation between populations and between sexes was primarily located in the cranial region, within-sex variation was relatively uniform across all landmarks.

Conclusions

Deviations of the between-population and between-sex pattern of shape variation from that within sex indicate that the differences in head shape likely result from both adaptations to female mouthbrooding and population-specific foraging strategies.

Background

Asymmetry in animal bodies and behavior has evolved several times, but our knowledge of their linkage is limited. Tanganyikan scale-eating cichlids have well-known antisymmetry in their bodies and behavior; individuals open their mouths leftward (righty) or rightward (lefty), and righties always attack the right flank of the prey, whereas lefties attack the left. This study analyzed the morphological asymmetry in a scale-eating characiform, Exodon paradoxus, and its behavioral handedness.

Methodology/Principal Findings

Each eight E. paradoxus was observed for 1-h with a prey goldfish in an aquarium to detect the behavioral handedness. Following the experiment, the lateral differences in the mandibles and head-inclination of these eight and ten additional specimens were analyzed. Both measurements on the morphology showed a bimodal distribution, and the laterality identified by these two methods was always consistent within a given individual, indicating that the characin has morphological antisymmetry. Furthermore, this laterality significantly corresponded to behavioral handedness; that is, lefties more often rasped scales from the right flank of the prey and vice versa. However, the correlation between laterality and handedness is the opposite of that in the cichlids. This is due to differences in the feeding apparatus and technique. The characin has cuspids pointing forward on the external side of the premaxilla, and it thrusts its dominant body side outward from its body axis on the flank of the prey to tear off scales. By contrast, the cichlids draw their dominant body side inward toward the axis or rotate it to scrape or wrench off scales with the teeth lined in the opened mouth.

Conclusions/Significance

This study demonstrated that the antisymmetry in external morphology and the corresponding behavioral handedness have evolved in two lineages of scale-eating fishes independently, and these fishes adopt different utilization of their body asymmetry to tear off scales.

Background

How particular changes in functional morphology can repeatedly promote ecological diversification is an active area of evolutionary investigation. The African rift-lake cichlids offer a calibrated time series of the most dramatic adaptive radiations of vertebrate trophic morphology yet described, and the replicate nature of these events provides a unique opportunity to test whether common changes in functional morphology have repeatedly facilitated their ecological success.

Methodology/Principal Findings

Specimens from 87 genera of cichlid fishes endemic to Lakes Tanganyka, Malawi and Victoria were dissected in order to examine the functional morphology of cichlid feeding. We quantified shape using geometric morphometrics and compared patterns of morphological diversity using a series of analytical tests. The primary axes of divergence were conserved among all three radiations, and the most prevalent changes involved the size of the preorbital region of the skull. Even the fishes from the youngest of these lakes (Victoria), which exhibit the lowest amount of skull shape disparity, have undergone extensive preorbital evolution relative to other craniofacial traits. Such changes have large effects on feeding biomechanics, and can promote expansion into a wide array of niches along a bentho-pelagic ecomorphological axis.

Conclusions/Significance

Here we show that specific changes in trophic anatomy have evolved repeatedly in the African rift lakes, and our results suggest that simple morphological alterations that have large ecological consequences are likely to constitute critical components of adaptive radiations in functional morphology. Such shifts may precede more complex shape changes as lineages diversify into unoccupied niches. The data presented here, combined with observations of other fish lineages, suggest that the preorbital region represents an evolutionary module that can respond quickly to natural selection when fishes colonize new lakes. Characterizing the changes in cichlid trophic morphology that have contributed to their extraordinary adaptive radiations has broad evolutionary implications, and such studies are necessary for directing future investigations into the proximate mechanisms that have shaped these spectacular phenomena.

Morphological dimorphism in the mouth-opening direction (‘lefty’ versus ‘righty’) has been documented in several fish species. It has been suggested that this deflection is heritable in a Mendelian one-locus, two-allele fashion. Several population models have demonstrated that lateral dimorphism is maintained by negative frequency-dependent selection, resulting from interactions between predator and prey species. However, other mechanisms for the maintenance of lateral dimorphism have not yet been tested. Here, we found that the scale-eating cichlid fish Perissodus microlepis exhibited disassortative mating, in which reproductive pairings between lefties and righties occurred at higher than expected frequency (p<0.001). A previous study reported that a lefty–righty pairing produces a 1 : 1 ratio of lefty : righty young, suggesting that disassortative mating contributes to the maintenance of lateral dimorphism. A combination of disassortative mating and negative frequency-dependent selection may stabilize lateral dimorphism more than would a single mechanism.

One of the most compelling features of the cichlid fishes of the African Great Lakes is the seemingly endless diversity of male coloration. Colour diversification has been implicated as an important factor driving cichlid speciation. Colour has also been central to cichlid taxonomy and, thus, to our concept of species diversity. We undertook a phylogeographical examination of several allopatric populations of the Lake Malawi cichlid Pseudotropheus zebra in order to reconstruct the evolutionary history of the populations, which exhibit one of two dorsal fin colours. We present evidence that populations with red dorsal fins (RT) are not monophyletic. The RT population defining the northern limit of the distribution has evidently originated independently of the southern RT populations, which share a common ancestry. This evidence of species-level colour convergence is an important discovery in our understanding of cichlid evolution. It implies that divergence in coloration may accompany speciation, and that allopatric populations with similar coloration cannot be assumed to be conspecific. In addition to this finding, we have observed evidence for introgression, contributing to current evidence that this phenomenon may be extremely widespread. Thus, in species-level phylogenetic reconstructions, including our own, consideration must be given to the potential effects of introgression.