Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fish Perissodus microlepis

The scale‐eating cichlid fish Perissodus microlepis is a textbook example of bilateral asymmetry due to its left or right‐bending heads and of negative frequency‐dependent selection, which is proposed to maintain this stable polymorphism. The mechanisms that underlie this asymmetry remain elusive. Several studies had initially postulated a simple genetic basis for this trait, but this explanation has been questioned, particularly by reports observing a unimodal distribution of mouth shapes. We hypothesize that this unimodal distribution might be due to a combination of genetic and phenotypically plastic components. Here, we expanded on previous work by investigating a formerly identified candidate SNP associated to mouth laterality, documenting inter‐individual variation in feeding preference using stable isotope analyses, and testing their association with mouth asymmetry. Our results suggest that this polymorphism is influenced by both a polygenic basis and inter‐individual non‐genetic variation, possibly due to feeding experience, individual specialization, and intraspecific competition. We introduce a hypothesis potentially explaining the simultaneous maintenance of left, right, asymmetric and symmetric mouth phenotypes due to the interaction between diverse eco‐evolutionary dynamics including niche construction and balancing selection. Future studies will have to further tease apart the relative contribution of genetic and environmental factors and their interactions in an integrated fashion.     

Genetic and environmental effects on the morphological asymmetry in the scale‐eating cichlid fish,Perissodus microlepis

The scale‐eating cichlid fish, Perissodus microlepis, from Lake Tanganyika are a well‐known example of an asymmetry dimorphism because the mouth/head is either left‐bending or right‐bending. However, how strongly its pronounced morphological laterality is affected by genetic and environmental factors remains unclear. Using quantitative assessments of mouth asymmetry, we investigated its origin by estimating narrow‐sense heritability (h²) using midparent–offspring regression. The heritability estimates [field estimate: h² = 0.22 ± 0.06, P = 0.013; laboratory estimate: h² = 0.18 ± 0.05, P = 0.004] suggest that although variation in laterality has some additive genetic component, it is strongly environmentally influenced. Family‐level association analyses of a putative microsatellite marker that was claimed to be linked to gene(s) for laterality revealed no association of this locus with laterality. Moreover, the observed phenotype frequencies in offspring from parents of different phenotype combinations were not consistent with a previously suggested single‐locus two‐allele model, but they neither were able to reject with confidence a random asymmetry model. These results reconcile the disputed mechanisms for this textbook case of mouth asymmetry where both genetic and environmental factors contribute to this remarkable case of morphological asymmetry.     

Neolamprologus cancellatus, a new cichlid fish from Lake Tanganyika, Africa

Neolamprologus cancellatus, a new cichlid species, is described on the basis of eight specimens from the Zambian coast of Lake Tanganyika. The new species is characterized by a subtruncate caudal fin and a body that is slender (depth 22.3–25.2% in standard length) and easily distinguishable from its congeners by having 7–8 anal fin spines, 34–37 scales in longitudinal line, 33 total vertebrae, and a gridlike body pattern on a pale brownish body color. This species is only known to inhabit the shallow (2–7 m depth), rocky bottom of Wonzye Point in the southern part of the lake.     

Measuring and evaluating morphological asymmetry in fish: distinct lateral dimorphism in the jaws of scale‐eating cichlids

The left–right asymmetry of scale‐eating Tanganyikan cichlids is described as a unilateral topographical shift of the quadratomandibular joints. This morphological laterality has a genetic basis and has therefore been used as a model for studying negative frequency‐dependent selection and the resulting oscillation in frequencies of two genotypes, lefty and righty, in a population. This study aims were to confirm this laterality in Perissodus microlepis Boulenger and P. straeleni (Poll) and evaluate an appropriate method for measuring and testing the asymmetry. Left–right differences in the height of the mandible posterior ends (HMPE) and the angle between the neurocranium and vertebrae of P. microlepis and P. straeleni were measured on skeletal specimens. Snout‐bending angle was also measured using a dorsal image of the same individuals following a previous method. To define which distribution model, fluctuating asymmetry (FA), directional asymmetry (DA), or antisymmetry (AS), best fit to the lateral asymmetry of the traits, we provided an R package, IASD. As a result, HMPE and neurocranium–vertebrae angle of both species were best fitted to AS, suggesting that P. microlepis and P. straeleni showed a distinct dimorphism in these traits, although snout‐bending angle of P. microlepis was best fitted to FA. Measurement error was low for HMPE comparing the snout‐bending angle in P. microlepis, indicating that measuring HMPE is a more accurate method. The scale‐eating tribe Perissodini showed distinct antisymmetry in the jaw skeleton and neurocranium–vertebrae angle, and this laterality remains a valid marker for further evolutionary studies.     

Genetic support for random mating between left and right‐mouth morphs in the dimorphic scale‐eating cichlid fish Perissodus microlepis from Lake Tanganyika

Population genetic analyses were conducted to investigate whether random mating occurs between left and right‐mouth morphs of the dimorphic scale‐eating cichlid fish Perissodus microlepis from two geographical sites in southern Lake Tanganyika. The mitochondrial and nuclear DNA markers (13 microsatellite loci) revealed no genetic differentiation between left and right morphs (i.e. widespread interbreeding). The observed lack of genetic divergence between the different morphs allowed for the exclusion of the possibility of assortative mating between same morph types. The microsatellite data showed no significant departures of heterozygosity from Hardy–Weinberg equilibrium, suggesting purely random mating between the morphs. Overall, this study indicated no genetic evidence for either assortative or disassortative mating, but it did provide support for the random mating hypothesis. Highly significant, albeit weak, spatial population structure was also found when samples of different morphs were pooled according to geographical sites. An additional analysis of two microsatellite loci that were recently suggested to be putatively linked to the genetic locus that determines the laterality of these mouth morphs did not show any such association.     

Microdontochromis rotundiventralis, a new cichlid fish (perciformes: Cichlidae) from Lake Tanganyika

Microdontochromis rotundiventralis, a new species of cichlid fish, is described on the basis of 13 specimens from Nkumbula Island, Lake Tanganyika (Zambia). It is distinct from its only congener,M. tenuidentatus, in having two (rarely one) rows of teeth on both jaws, a rounded distal margin on the pelvic fin, the outermost pelvic fin soft ray length 1.23–1.43 times the innermost ray, a deeper body (depth 26.8–29.1% standard length) and the anal fin with 9 (rarely 8 or 10) soft rays.     

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.     

Mouth asymmetry in the textbook example of scale-eating cichlid fish is not a discrete dimorphism after all

Individuals of the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika tend to have remarkably asymmetric heads that are either left-bending or right-bending. The ‘left’ morph opens its mouth markedly towards the left and preferentially feeds on the scales from the right-hand side of its victim fish, and the ‘right’ morph bites scales from the victims’ left-hand side. This striking dimorphism made these fish a textbook example of their astonishing degree of ecological specialization and as one of the few known incidences of negative frequency-dependent selection acting on an asymmetric morphological trait, where left and right forms are equally frequent within a species. We investigated the degree and the shape of the frequency distribution of head asymmetry in P. microlepis to test whether the variation conforms to a discrete dimorphism, as generally assumed. In both adult and juvenile fish, mouth asymmetry appeared to be continuously and unimodally distributed with no clear evidence for a discrete dimorphism. Mixture analyses did not reveal evidence of a discrete or even strong dimorphism. These results raise doubts about previous claims, as reported in textbooks, that head variation in P. microlepis represents a discrete dimorphism of left- and right-bending forms. Based on extensive field sampling that excluded ambiguous (i.e. symmetric or weakly asymmetric) individual adults, we found that left and right morphs occur in equal abundance in five populations. Moreover, mate pairing for 51 wild-caught pairs was random with regard to head laterality, calling into question reports that this laterality is maintained through disassortative mating.     

Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika

Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the ‘stages model’ of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation.     

Evidence for genetic monogamy and female-biased dispersal in the biparental mouthbrooding cichlid Eretmodus cyanostictus from Lake Tanganyika

In this study, we investigate whether apparent social monogamy (where a species forms a pair bond but may participate in copulations outside the pair bond) corresponds with genetic monogamy (where individuals participate only in copulations within a pair bond) in a biparental mouthbrooding cichlid fish, Eretmodus cyanostictus, from Lake Tanganyika, Africa. Our findings suggest that E. cyanostictus is both socially and genetically monogamous and that monogamy may result from limited opportunities for polygyny, rather than from reproductive benefits of monogamy. Mating systems are believed to influence the relative rate of dispersal of the sexes, and our results suggest that E. cyanostictus displays female-biased dispersal, providing some support for the 'resource competition' hypothesis driving sex-biased dispersal.     

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.     

Mating system and kin relationship between adults and young in the shell-brooding cichlid fish <Emphasis Type="Italic">Neolamprologus meeli</Emphasis> in Lake Tanganyika

Mating system and parental behavior of ten monogamous pairs and two polygynous groups of the Tanganyikan cichlid Neolamprologus meeli were observed in their natural habitat. The home ranges of males and females overlapped with each other. Most groups included one to six young. Paternal and maternal relationships were determined for 22 young from DNA microsatellite markers. Three types of kinship were found: (I) kinship to both the male and female; (II) kinship to females only; and (III) non-kinship to both sexes. In the groups with type II young, step-fathering or sneaking may have occurred. Type III young were larger than type I, suggesting that the former were of sufficient size to leave their birth nest and settle in the territories of foster parents. Both males and females drove out potential predators of young (including three species of Lepidiolamprologus) as a parental behavior. Adults with type III young attacked approaching predators with as much frequency as those with type I young only, indicating that they provided alloparental care. Adults and young swam together, but, a significant difference existed in the frequencies of interactions between adults versus kin young and adults versus non-kin young. The results suggest that both adults and young recognized kin. Electronic Publication     

Community assembly in Lake Tanganyika cichlid fish: quantifying the contributions of both niche‐based and neutral processes

The cichlid family features some of the most spectacular examples of adaptive radiation. Evolutionary studies have highlighted the importance of both trophic adaptation and sexual selection in cichlid speciation. However, it is poorly understood what processes drive the composition and diversity of local cichlid species assemblages on relatively short, ecological timescales. Here, we investigate the relative importance of niche‐based and neutral processes in determining the composition and diversity of cichlid communities inhabiting various environmental conditions in the littoral zone of Lake Tanganyika, Zambia. We collected data on cichlid abundance, morphometrics, and local environments. We analyzed relationships between mean trait values, community composition, and environmental variation, and used a recently developed modeling technique (STEPCAM) to estimate the contributions of niche‐based and neutral processes to community assembly. Contrary to our expectations, our results show that stochastic processes, and not niche‐based processes, were responsible for the majority of cichlid community assembly. We also found that the relative importance of niche‐based and neutral processes was constant across environments. However, we found significant relationships between environmental variation, community trait means, and community composition. These relationships were caused by niche‐based processes, as they disappeared in simulated, purely neutrally assembled communities. Importantly, these results can potentially reconcile seemingly contrasting findings in the literature about the importance of either niche‐based or neutral‐based processes in community assembly, as we show that significant trait relationships can already be found in nearly (but not completely) neutrally assembled communities; that is, even a small deviation from neutrality can have major effects on community patterns.     

Geometric morphometrics applied to viscerocranial bones in three populations of the Lake Tanganyika cichlid fish Tropheus moorii

Lake Tanganyika comprises the oldest and most diverse species flock of cichlid fishes. Many species are subdivided into numerous populations, often classified as geographical races, colour morphs or sister species. Unlike younger species flocks, in which speciation is accompanied by eco-morphological diversification that of Lake Tanganyika is at a mature stage with little further morphological change, most probably caused by stabilizing selection. This study addresses body shape differences among three genetically distinct but morphologically similar populations of Tropheus  moorii , by focusing on bony structures of the cichlid head. We test by means of geometric morphological methods whether shape changes in the cichlid head are based on particular osteological differences. Specimens were disarticulated enzymatically, and standardized digital images of the disarticulated bony elements were taken. A landmark system was established for the dentary, articular, premaxilla, quadrate and the preopercle. Only the dentary shows significant differentiation among the three populations. Since all three populations live in similar cobble habitats and occupy the same trophic niche, the observed difference in the shape of the dentary can either be explained by different directional selection due to subtle habitat differences, or by neutral drift constrained by borders enforced through stabilizing selection. Lack of difference might indicate stabilizing selection on bone shape.     

Variation of anal fin egg‐spots along an environmental gradient in a haplochromine cichlid fish

Male secondary sexual traits are targets of inter‐ and/or intrasexual selection, but can vary due to a correlation with life‐history traits or as by‐product of adaptation to distinct environments. Trade‐offs contributing to this variation may comprise conspicuousness toward conspecifics versus inconspicuousness toward predators, or between allocating resources into coloration versus the immune system. Here, we examine variation in expression of a carotenoid‐based visual signal, anal‐fin egg‐spots, along a replicate environmental gradient in the haplochromine cichlid fish Astatotilapia burtoni. We quantified egg‐spot number, area, and coloration; applied visual models to estimate the trait's conspicuousness when perceived against the surrounding tissue under natural conditions; and used the lymphocyte ratio as a measure for immune activity. We find that (1) males possess larger and more conspicuous egg‐spots than females, which is likely explained by their function in sexual selection; (2) riverine fish generally feature fewer but larger and/or more intensely colored egg‐spots, which is probably to maintain signal efficiency in intraspecific interactions in long wavelength shifted riverine light conditions; and (3) egg‐spot number and relative area correlate with immune defense, suggesting a trade‐off in the allocation of carotenoids. Taken together, haplochromine egg‐spots feature the potential to adapt to the respective underwater light environment, and are traded off with investment into the immune system.     

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.     

Resource-based adaptive divergence in the freshwater fish Telmatherina from Lake Matano, Indonesia

Adaptive radiations are an important source of biodiversity, but resolving which ecological pressures seed these processes in natural systems remains difficult. Here the adaptive radiation among Telmatherina, a genus of freshwater fish endemic to an ancient lake in central Sulawesi, Indonesia, was examined to determine its causal root. We demonstrate that all Telmatherina in this lake can be categorized into three lineages each possessing specialized skull shapes and pharyngeal jaw bones allowing them to exploit different resources. These data demonstrate a natural example of how resource partitioning has likely initiated adaptive radiation in a resource limited environment.