Validation of the periodicity of increment formation in the otoliths of a cichlid fish from Lake Tanganyika, East Africa

Tetracycline was used as a chemical tag in a mark‐recapture study to examine the pattern of increment formation in the otoliths of Tropheus moorii , a rock‐dwelling cichlid from Lake Tanganyika. A total of 256 fish were captured by divers and injected with tetracycline. Of these, nine were recaptured after either 1 or 2 years at liberty and eight retained tags within their otoliths. Comparison of the number of growth increments formed after the tag and the time at liberty demonstrated that increments were deposited on an annual basis in the otoliths of this species. Furthermore, there was a strong relationship between otolith mass and age suggesting that otoliths grew at a predictable rate throughout the life of the fish. Validation of an annual pattern of increment deposition allowed age and growth information to be derived from otoliths. This showed that T. moorii grew rapidly to attain adult size by 3 years of age. Males grew faster than females and also attained a larger size than females (8·74 v . 7·91 cm L _S respectively). The longevity of some of these small freshwater fish was surprising; the oldest individual had an age of 10 years, while the average age of adults was 4 years.     

Monogamy in the maternally mouthbrooding Lake Tanganyika cichlid fish Tropheus moorii

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.     

Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika

The conditions of phenotypic and genetic population differentiation allow inferences about the evolution, preservation and loss of biological diversity. In Lake Tanganyika, water level fluctuations are assumed to have had a major impact on the evolution of stenotopic littoral species, though this hypothesis has not been specifically examined so far. The present study investigates whether subtly differentiated colour patterns of adjacent Tropheus moorii populations are maintained in isolation or in the face of continuous gene flow, and whether the presumed influence of water level fluctuations on lacustrine cichlids can be demonstrated in the small-scale population structure of the strictly stenotopic, littoral Tropheus. Distinct population differentiation was found even across short geographic distances and minor habitat barriers. Population splitting chronology and demographic histories comply with our expectation of old and rather stable populations on steeper sloping shore, and more recently established populations in a shallower region. Moreover, population expansions seem to coincide with lake level rises in the wake of Late Pleistocene megadroughts ~100 KYA. The imprint of hydrologic events on current population structure in the absence of ongoing gene flow suggests that phenotypic differentiation among proximate Tropheus populations evolves and persists in genetic isolation. Sporadic gene flow is effected by lake level fluctuations following climate changes and controlled by the persistence of habitat barriers during lake level changes. Since similar demographic patterns were previously reported for Lake Malawi cichlids, our data furthermore strengthen the hypothesis that major climatic events synchronized facets of cichlid evolution across the East African Great Lakes.     

Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika

Several lineages of cichlid fishes in the East African Great Lakes display stunning levels of morphological diversification. The rapid evolution of rock-dwelling polygynous mouthbrooders in Lake Malawi, for example, was in part ascribed to their allopatric distribution on disjunct stretches of rocky coast, where even short habitat discontinuities reduce gene flow effectively. However, as seen in other cichlids, ecological barriers do not always prevent gene flow, whereas genetic structure can develop along continuous habitat, and morphological diversification does not necessarily accompany genetic differentiation. The present study investigates the population structure of Variabilichromis moorii, a monogamous substrate-brooding lamprologine of rocky coasts in Lake Tanganyika, which occurs over about 1000 km of shoreline almost without phenotypic variation. Phylogeographic analyses of mitochondrial DNA sequences indicated that dispersal is infrequent and generally occurs between adjacent locations only. Exceptions to this pattern are closely related haplotypes from certain locations on opposite lakeshores, a phenomenon which has been observed in other species and is thought to reflect lake crossing along an underwater ridge in times of low water level. Genetic population differentiation, estimated from mitochondrial DNA and microsatellite data in six adjacent populations, was equally high across localities separated by sandy shores and along uninterrupted stretches of rocky shore. Our results suggest that ecological barriers are not required to induce philopatric behavior in Variabilichromis, and that morphological stasis persists in the face of high levels of neutral genetic differentiation.     

Evolution of body shape in sympatric versus non-sympatric Tropheus populations of Lake Tanganyika

Allopatric speciation often yields ecologically equivalent sister species, so that their secondary admixis enforces competition. The shores of Lake Tanganyika harbor about 120 distinct populations of the cichlid genus Tropheus, but only some are sympatric. When alone, Tropheus occupies a relatively broad depth zone, but in sympatry, fish segregate by depth. To assess the effects of competition, we studied the partial co-occurrence of Tropheus moorii ‘Kaiser'' and ‘Kirschfleck'' with Tropheus polli. A previous study demonstrated via standardized breeding experiments that some observed differences between Tropheus ‘Kaiser'' living alone and in sympatry with T. polli have a genetic basis despite large-scale phenotypic plasticity. Using geometric morphometrics and neutral genetic markers, we now investigated whether sympatric populations differ consistently in body shape from populations living alone and if the differences are adaptive. We found significant differences in mean shape between non-sympatric and sympatric populations, whereas all sympatric populations of both color morphs clustered together in shape space. Sympatric populations had a relatively smaller head, smaller eyes and a more anterior insertion of the pectoral fin than non-sympatric populations. Genetically, however, non-sympatric and sympatric ‘Kaiser'' populations clustered together to the exclusion of ‘Kirschfleck''. Genetic distances, but not morphological distances, were correlated with geographic distances. Within- and between-population covariance matrices for T. moorii populations deviated from proportionality. It is thus likely that natural selection acts on both phenotypic plasticity and heritable traits and that both factors contribute to the observed shape differences. The consistency of the pattern in five populations suggests ecological character displacement.     

Geometric morphometrics: recent applications to the study of evolution and development

The field of morphometrics is developing quickly and recent advances allow for geometric techniques to be applied easily to many zoological problems. This paper briefly introduces geometric morphometric techniques and then reviews selected areas where those techniques have been applied to questions of general interest. This paper is relevant to non-specialists looking for an entry into geometric morphometric methods and for ideas of how to incorporate them into the study of variation within and between species, the measurement of developmental stability, the role of development in shaping evolution and the special problem of measuring the shape of fossil specimens that are deformed from their original shape.     

Evidence for divergent natural selection of a Lake Tanganyika cichlid inferred from repeated radiations in body size

Divergent natural selection is thought to play a vital role in speciation, but clear, measurable examples from nature are still few. Among the many possible sources of divergent natural selection, predation pressure may be important because predators are ubiquitous in food webs. Here, we show evidence for divergent natural selection in a Lake Tanganyika cichlid, Telmatochromis temporalis , which uses burrows under stones or empty snail shells as shelters. This species contains normal and dwarf morphs at several localities. The normal morph inhabits rocky shorelines, whereas the dwarf morph invariably inhabits shell beds, where empty snail shells densely cover the lake bottom. Genetic evidence suggested that the dwarf morph evolved independently from the normal morph at two areas, and morphological analysis and evaluation of habitat structure revealed that the body sizes of morphs closely matched the available shelter sizes in their habitats. These findings suggest that the two morphs repeatedly evolved through divergent natural selection associated with the strategy for sheltering from predators.     

Body size evolution of a shell‐brooding cichlid fish from Lake Tanganyika

The substrate‐brooding cichlid fish Telmatochromis temporalis in Lake Tanganyika demonstrates a simple example of ecological speciation between normal and dwarf morphs through divergent natural selection on body size. The dwarf morph most likely evolved from the ancestral normal morph; therefore, elucidating the evolution of its small body size is a key to understanding this ecological speciation event. Previous studies suggest that the small body size of the dwarf morph is an adaptation to the use of empty snail shells as shelters (males) and spawning sites (females), but this idea has not been fully evaluated. Combining original and previously published information, this study compared likelihood values to determine the primary factor that would be responsible for regulating the body size of the dwarf morph. Male body size is most likely regulated by the ability to turn within shells, which may influence the predation avoidance of adult fish. Females are smaller than males, and their body size is most likely regulated by the ability to lay eggs in the small spaces within shells close to the shell apices where predation risk on eggs is lower. This study provides new evidence supporting the hypothesis that different natural selection factors affected body size of the different sexes of the dwarf morph, which has not been reported in other animal species.     

Group foraging by the herbivorous cichlid fish,Petrochromis fasciolatus,in Lake Tanganyika

Group foraging of the algae eating cichlid,Petrochromis fasciolatus, was studied along a rocky shore in Lake Tanganyika, in an area occupied by the feeding territories of several herbivorous cichlid species. SolitaryP. fasciolatus or schools comprising a few members only were nearly always repelled from such territories, although larger schools (40–250 individuals) ofP. fasciolatus were able to overwhelm the defenses of territory owners and enable subsequent foraging. The frequency and duration of individual foraging sessions on the algal mats were positively correlated with group size, probably owing to individuals in large schools suffering fewer attacks from territory owners. Almost all of the foraging sites ofP. fasciolatus were inside the territories of other herbivorous cichlids, especially those ofNeolamprologus moorii (more than 80% of total), in which the algal density was more than 10 times that in territories of the other species.N. moorii territories included only 4% rocky substrate, indicating that schools ofP. fasciolatus selectively chose territories containing rich resources.     

Evolution of a cichlid fish in a Lake Malawi satellite lake

Allopatric divergence in peripheral habitats may lead to rapid evolution of populations with novel phenotypes. In this study we provide the first evidence that isolation in peripheral habitats may have played a critical role in generation of Lake Malawi's cichlid fish diversity. We show that Lake Chilingali, a satellite lake 11.5 km from the shore of Lake Malawi, contains a breeding population of Rhamphochromis, a predatory genus previously thought to be restricted to Lake Malawi and permanently connected water bodies. The Lake Chilingali population is the smallest known Rhamphochromis, has a unique male nuptial colour pattern and has significant differentiation in mitochondrial DNA from Lake Malawi species. In laboratory mate choice trials with a candidate sister population from Lake Malawi, females showed a strong tendency to mate assortatively indicating that they are incipient biological species. These data support the hypothesis that isolation and reconnection of peripheral habitats due to lake level changes have contributed to the generation of cichlid diversity within African lakes. Such cycles of habitat isolation and reconnection may also have been important in evolutionary diversification of numerous other abundant and wide-ranging aquatic organisms, such as marine fishes and invertebrates.     

Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations

The cichlids of East Africa are renowned as one of the most spectacular examples of adaptive radiation. They provide a unique opportunity to investigate the relationships between ecology, morphological diversity, and phylogeny in producing such remarkable diversity. Nevertheless, the parameters of the adaptive radiations of these fish have not been satisfactorily quantified yet. Lake Tanganyika possesses all of the major lineages of East African cichlid fish, so by using geometric morphometrics and comparative analyses of ecology and morphology, in an explicitly phylogenetic context, we quantify the role of ecology in driving adaptive speciation. We used geometric morphometric methods to describe the body shape of over 1000 specimens of East African cichlid fish, with a focus on the Lake Tanganyika species assemblage, which is composed of more than 200 endemic species. The main differences in shape concern the length of the whole body and the relative sizes of the head and caudal peduncle. We investigated the influence of phylogeny on similarity of shape using both distance-based and variance partitioning methods, finding that phylogenetic inertia exerts little influence on overall body shape. Therefore, we quantified the relative effect of major ecological traits on shape using phylogenetic generalized least squares and disparity analyses. These analyses conclude that body shape is most strongly predicted by feeding preferences (i.e., trophic niches) and the water depths at which species occur. Furthermore, the morphological disparity within tribes indicates that even though the morphological diversification associated with explosive speciation has happened in only a few tribes of the Tanganyikan assemblage, the potential to evolve diverse morphologies exists in all tribes. Quantitative data support the existence of extensive parallelism in several independent adaptive radiations in Lake Tanganyika. Notably, Tanganyikan mouthbrooders belonging to the C-lineage and the substrate spawning Lamprologini have evolved a multitude of different shapes from elongated and Lamprologus-like hypothetical ancestors. Together, these data demonstrate strong support for the adaptive character of East African cichlid radiations.     

Mouth dimorphism in scale‐eating cichlid fish from Lake Tanganyika advances individual fitness

Random asymmetry, that is the coexistence of left‐ and right‐sided (or ‐handed) individuals within a population, is a particular case of natural variation; what triggers and maintains such dimorphisms remains unknown in most cases. Here, we report a field‐based cage experiment in the scale‐eating Tanganyikan cichlid Perissodus microlepis, which occurs in two morphs in nature: left‐skewed and right‐skewed individuals with respect to mouth orientation. Using underwater cages stocked with scale‐eaters and natural prey fish, we first confirm that, under semi‐natural conditions, left‐skewed scale‐eaters preferentially attack the right flank of their prey, whereas right‐skewed individuals feed predominantly from the left side. We then demonstrate that scale‐eaters have a higher probability for successful attacks when kept in dimorphic experimental populations (left‐ and right‐skewed morphs together) as compared to monomorphic populations (left‐ or right‐skewed morphs), most likely because prey fishes fail to accustom to strikes from both sides. The significantly increased probability for attacks appears to be the selective agent responsible for the evolution and maintenance of mouth dimorphism in P. microlepis, lending further support to the hypothesis that negative frequency‐dependent selection is the stabilizing force balancing the mouth dimorphism at quasi‐equal ratios in scale‐eating cichlids.     

Overlapping territory of the benthophagous cichlid fish, Lobochilotes labiatus, in Lake Tanganyika

Synopsis Feeding territories do not usually overlap in the same fish species. We studied overlapping territories and feeding behaviours of a benthophagous cichlid fish Lobochilotes labiatus Boulenger in a coastal area of Lake Tanganyika. Forty-four individuals of both sexes, 6–31 cm in total length, maintained territories in a 21 m × 25 m area. These could be regarded as feeding territories. The territories of similar-sized owners (usually different by less than 5 cm) did not overlap each other, but those of different-sized owners overlapped widely. Aggressive interactions were rarely observed between fish distinctly different in body size. Both large and small fish took benthic animals of the same kinds and of similar size. In contrast, the size of foraging sites (crevices) was different between them: the large fish foraged at large crevices and small fish at small crevices. This partitioning of foraging sites may enable the overlap of territories in this benthivore.     

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.     

Context‐dependent expression of sexual dimorphism in island populations of the common wall lizard (Podarcis muralis)

The condition‐dependent sexual dimorphism model explains the evolution and maintenance of sexual dimorphism in traits targeted by sexual selection, and predicts that the magnitude of sexual dimorphism depends on the variability of individual condition, male traits being more variable than female corresponding traits. Most convincing examples concern insects, while studies among vertebrates are scanty because manipulating condition often is not possible, and the time to reach sexual maturity may be too long. Islands offer a unique opportunity to compare how the environment affects the expression of sexual dimorphism, since they represent ‘natural experimental sets’ in which different populations of the same species may experience alternative environmental constraints. We investigated the occurrence of context‐dependent expression in sexual dimorphism of head shape in insular populations of the common wall lizards (Podarcis muralis) inhabiting the Tuscan Archipelago (Tyrrhenian Sea). Alternative models were formulated: H₀ assumes that the sexual dimorphism is uninfluenced by islands, H₁ assumes the only effect of phylogeny, H_2A and H_2B account for the biogeography of the archipelago (island size and distance from the mainland), while H₃ assumes island‐specific effects on sexual dimorphism. Models were compared using Akaike's information criterion adjusted for multivariate analyses. All hypotheses performed better than H₀, but H₃ largely outperformed all other alternative hypotheses, indicating that environmental features of islands play an additive effect to ontogenetic, biogeographic and genetic factors in defining variation in head shape sexual dimorphism. Our results support the hypothesis of a context‐dependent sexual dimorphism in common wall lizards. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 552–565.     

Exploring sexual dimorphism of human occipital and temporal bones through geometric morphometrics in an identified Western-European sample

Sex estimation is a paramount step of bioprofiling in both forensic anthropology and osteoarchaeology. When the pelvis is not optimally preserved, anthropologists commonly rely on the cranium to accurately estimate sex. Over the last decades, the geometric morphometric (GM) approach has been used to determine sexual dimorphism of the crania, in size and shape, overcoming some difficulties of traditional visual and metric methods. This article aims to investigate sexual dimorphism of the occipital and temporal region through GM analysis in a metapopulation of 50 Western-European identified individuals. Statistical analyses were performed to compare centroid size and shape data between sexes through the examination of distinct functional modules. Regression and Procrustes ANOVA were used to examine allometric and asymmetrical implications. Discriminant functions, combining size and shape data, were established. Significant dimorphism in size was found, with males having larger crania, confirming the major influence size has on cranial morphology. Allometric relationships were found to be statistically significant in both right and left temporal bones while shape differences between sexes were only significant on the right temporal bone. The visualization of the mean consensus demonstrated that males displayed a larger mastoid process associated with a reduced mastoid triangle and less projected occipital condyles. This exploratory study confirms that GM analysis represents an effective way to quantitatively capture shape of dimorphic structures, even on complex rounded ones such as the mastoid region. Further examination in a larger sample would be valuable to design objective visualization tools that can improve morphoscopic sex estimation methods.