Magadi tilapia ecological specialization: filling the early gap in the speciation continuum

Cichlid fish are well known for their high speciation rates, which are usually accompanied by spectacular and rapid diversification in eco‐morphological and secondary sexual traits. This is best illustrated by the famous repeated explosive radiations in the African Great Lakes Tanganyika, Malawi and Victoria, each lake harbouring several hundreds of mostly endemic species. Correspondingly, cichlids diversified very rapidly in many other lakes across their range. Although the larger radiations, unparalleled in vertebrates, are certainly the most intriguing, they are also the most intricate and difficult to address because of their complex nature. This is where smaller, simpler systems may prove to be the most useful. In this issue of Molecular Ecology, Kavembe et al. ( 2016 ) report very recent genetic diversification accompanied by ecological specialization in cichlids of the small and ecologically extreme Lake Magadi, in Kenya. Combining geometric morphometrics, stable isotope analysis, population genomics using RADSeq data and coalescent‐based modelling techniques, the authors characterize the eco‐morphological differences between genetically distinct populations of Magadi tilapia (Alcolapia grahami), which are consistent with the different environmental conditions they experience, and infer their history of divergence. The simplicity of the focal system and the use of a multidisciplinary approach make this work particularly important for our understanding of the early stages of speciation, in both cichlids and other organisms.     

Modelling of essential fish habitat based on remote sensing,spatial analysis and GIS

Lake Tanganyika is not the most species-rich of the Great East African Lakes, but comprises the greatest diversity of cichlid fishes in terms of morphology, ecology, and breeding styles. The lake contains a polyphyletic assemblage of cichlid lineages, which evolved from several ancient species that colonized the emerging lake some 9–12 million years ago. Based on morphological characteristics, the Tanganyikan cichlids have been classified into 12, or, more recently, 16 tribes, which are largely supported by molecular data. The radiations of East African cichlids are believed to be driven by complex interactions between extrinsic factors, such as climatic changes and geological processes, and intrinsic biological characteristics of the involved organisms. Diversification within different lineages occurred simultaneously in response to drastic habitat changes such as the establishment of lacustrine deep-water conditions 5–6 MYA and subsequent major lake-level fluctuations. This seems particularly true for the mouthbrooding lineages whereas the substrate breeders underwent a more gradual process of diversification. This review presents an account of the taxonomy and phylogeny of the Lake Tanganyika cichlid species assemblage, its relationship to the African cichlid fauna, key factors leading to the astonishing diversity and discusses recently proposed alternative age estimates for the Lake Tanganyika cichlid species assemblage.     

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.     

Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation

Background  

Phenotypic evolution and its role in the diversification of organisms is a central topic in evolutionary biology. A neglected factor during the modern evolutionary synthesis, adaptive phenotypic plasticity, more recently attracted the attention of many evolutionary biologists and is now recognized as an important ingredient in both population persistence and diversification. The traits and directions in which an ancestral source population displays phenotypic plasticity might partly determine the trajectories in morphospace, which are accessible for an adaptive radiation, starting from the colonization of a novel environment. In the case of repeated colonizations of similar environments from the same source population this "flexible stem" hypothesis predicts similar phenotypes to arise in repeated subsequent radiations. The Midas Cichlid (Amphilophus spp.) in Nicaragua has radiated in parallel in several crater-lakes seeded by populations originating from the Nicaraguan Great Lakes. Here, we tested phenotypic plasticity in the pharyngeal jaw of Midas Cichlids. The pharyngeal jaw apparatus of cichlids, a second set of jaws functionally decoupled from the oral ones, is known to mediate ecological specialization and often differs strongly between sister-species.     

Shifting barriers and phenotypic diversification by hybridisation

The establishment of hybrid taxa relies on reproductive isolation from the parental forms, typically achieved by ecological differentiation. Here, we present an alternative mechanism, in which shifts in the strength and location of dispersal barriers facilitate diversification by hybridisation. Our case study concerns the highly diverse, stenotopic rock‐dwelling cichlids of the African Great Lakes, many of which display geographic colour pattern variation. The littoral habitat of these fish has repeatedly been restructured in the course of ancient lake level fluctuations. Genetic data and an experimental cross support the hybrid origin of a distinct yellow‐coloured variant of Tropheus moorii from ancient admixture between two allopatric, red and bluish variants. Deficient assortative mating preferences imply that reproductive isolation continues to be contingent on geographic separation. Linking paleolimnological data with the establishment of the hybrid variant, we sketch a selectively neutral diversification process governed solely by rearrangements of dispersal barriers.     

Molecular phylogeny and speciation patterns in host-specific monogeneans (Cichlidogyrus,Dactylogyridae) parasitizing cichlid fishes (Cichliformes,Cichlidae) in Lake Tanganyika

Cichlidogyrus (including Scutogyrus) is the most speciose dactylogyridean monogenean genus known from African and Levantine cichlid fishes (Cichlidae). While its taxonomy is well established, little is known about the phylogenetic relationships and evolutionary history of this ectoparasite, especially from hosts belonging to one of the most impressive vertebrate radiations, the cichlid fishes from the East African Great Lakes and surrounding hydrological systems. Phylogenetic inference based on DNA sequences of the nuclear 18S, internal transcribed spacer 1 and 28S rDNA genes revealed that Cichlidogyrus parasitizing mainly West African cichlid tribes is paraphyletic with respect to species parasitizing hosts belonging to the East African cichlid radiation, which constitute a well-supported monophylum. Members of Cichlidogyrus from tylochromine and oreochromine hosts that colonised Lake Tanganyika only recently, cluster with their non-Lake Tanganyika relatives, indicating that they colonised Lake Tanganyika with their current host species, and did not jump over from any of the many cichlid species already present in the lake. The diversification of Cichlidogyrus in Lake Tanganyika seems to be driven by failure to diverge in old lineages of cichlids, cospeciation in more recently evolved ones, and host switching followed by parasite duplication at the level of the various host tribes. Evaluation of host specificity and structural evolution of haptoral and reproductive organs in Lake Tanganyika Cichlidogyrus revealed that strict specialist species together with larval hook size represent the ancestral state of haptor configuration, suggesting that members of Cichlidogyrus in this system evolved from a very simple form to a more complex one similarly to their West African congeners. Generalist species among Cichlidogyrus with a sclerotized vagina parasitizing ancient Lake Tanganyika lineages seem to have developed a different hook configuration, most probably to ensure successful colonisation of new, phylogenetically unrelated hosts.     

Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes

Geographical isolation, habitat variation and trophic specialization have contributed to a large extent to the astonishing diversity of cichlid fishes in the Great East African lakes. Because parasite communities often vary across space and environments, parasites can accompany and potentially enhance cichlid species diversification. However, host dispersal may reduce opportunities for parasite‐driven evolution by homogenizing parasite communities and allele frequencies of immunity genes. To test for the relationships between parasite community variation, host dispersal and parasite‐induced host evolution, we studied two sympatric cichlid species with contrasting dispersal capacities along the shores of southern Lake Tanganyika. Whereas the philopatric Tropheus moorii evolved into several genetically differentiated colour morphs, Simochromis diagramma is phenotypically rather uniform across its distribution range and shows only weak population structure. Populations of both species were infected with divergent parasite communities and harbour differentiated variant pools of an important set of immune genes, the major histocompatibility complex (MHC). The overall extent of geographical variation of parasites and MHC genes was similar between host species. This indicates that immunogenetic divergence among populations of Lake Tanganyika cichlids can occur even in species that are strongly dispersing. However, because this also includes species that are phenotypically uniform, parasite‐induced evolution may not represent a key factor underlying species diversification in this system.     

Assortative mating preferences between colour morphs of the endemic Lake Tanganyika cichlid genus Tropheus

Female mate preferences effectuate reproductive isolation among and sexual selection within species. Both mechanisms have been associated with the diversification and speciation of cichlid species flocks of the East African Great Lakes. In Lake Tanganyika, the endemic genus Tropheus has diversified into >100 geographic colour morphs. Although distributed allopatrically at present, water level fluctuations have repeatedly displaced and merged the benthic, rock-dwelling populations. Tests for assortative mating were performed to explore the potential for reproductive isolation between morphs in secondary contact, and to assess the importance of sexual selection for the diversification of this group. In contrast to other haplochromine cichlids, Tropheus is a sexually monochromatic, territorial and maternally mouthbrooding fish, which establishes temporary pair bonds prior to spawning. Female mate preference trials involved two-way choices between a homotypic and a heterotypic male and were conducted on allopatric populations of red and blue morphs from the southern part of Lake Tanganyika. Female affiliation time near each male’s compartment did not predict the mate preferences subsequently expressed in unrestrained interactions after removal of the compartment separators (spawning, pseudospawning and courtship). Consequently, mate preferences were inferred from unrestrained interactions with one test male at a time in replicate observation sessions. Of the 23 females tested, 13 courted, pseudospawned or spawned with the homotypic male, one blue female courted a red male, and nine females expressed no sexual motivation. The assortative mate preferences in the experiments (P < 0.01) suggest that colour differentiation between Tropheus populations can effectuate reproductive isolation, and is consistent with the notion that sexual selection contributed to the diversification of the genus. Guest editors: T. Wilke, R. V?in?l? & F. Riedel Patterns and Processes of Speciation in Ancient Lakes: Proceedings of the Fourth Symposium on Speciation in Ancient Lakes, Berlin, Germany, September 4–8, 2006     

Relaxed trait covariance in interspecific cichlid hybrids predicts morphological diversity in adaptive radiations

The process of adaptive radiation involves multiple events of speciation in short succession, associated with ecological diversification. Understanding this process requires identifying the origins of heritable phenotypic variation that allows adaptive radiation to progress. Hybridization is one source of genetic and morphological variation that may spur adaptive radiation. We experimentally explored the potential role of hybridization in facilitating the onset of adaptive radiation. We generated first‐ and second‐generation hybrids of four species of African cichlid fish, extant relatives of the putative ancestors of the adaptive radiations of Lakes Victoria and Malawi. We compared patterns in hybrid morphological variation with the variation in the lake radiations. We show that significant fractions of the interspecific morphological variation and the major trajectories in morphospace that characterize whole radiations can be generated in second‐generation hybrids. Furthermore, we show that covariation between traits is relaxed in second‐generation hybrids, which may facilitate adaptive diversification. These results support the idea that hybridization can provide the heritable phenotypic diversity necessary to initiate adaptive radiation.     

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.     

Lacustrine radiations in African Synodontis catfish

Synodontis catfish are a species‐rich, tropical pan‐African genus that predominately occur in fluviatile environments, but which also form a small radiation within Lake Tanganyika (LT). Here we estimate Synodontis relationships, based on mitochondrial and nuclear DNA, greatly expanding previous sampling. Data were analysed using different methods of phylogenetic inference: Bayesian (also testing compositional heterogeneity), likelihood and parsimony, in order to investigate biogeographic history and the extent of intralacustrine speciation within this group. Bayesian‐relaxed clock analyses were used to estimate timings of radiations. Our analyses reveal a single origin of the LT flock with the inclusion of the nonendemic S. victoriae, and that these taxa evolved relatively recently (5.5 Ma), considerably later than the formation of LT (9–12 Ma). Two internal endemic clades diversified at a similar time (2–2.5 Ma), corresponding to a period of climate change, when lake levels dropped. We find evidence for a further species flock, composed of riverine southern African taxa, the diversification of which is very rapid, 0.8 Ma (95% HPD: 0.4–1.5) and infer a similar scenario for the diversification of this flock to southern African serrachromine cichlids in that they radiated in the now extinct lake Makgadikgadi. We also reveal that the biogeographic history of Synodontis catfish is more complex than previously thought, with nonmonophyletic geographic species groupings.     

Comparative rates of lower jaw diversification in cichlid adaptive radiations

The lower jaw (LJ) provides an ideal trophic phenotype to compare rates and patterns of macroevolution among cichlid radiations. Using a novel phylogeny of four genes (ND2, dlx2, mitfb, and s7), we examined the evolutionary relationships among two of the most phylogenetically disparate cichlid radiations: (i) the Central America Heroines; and (ii) the East African Lake Malawi flock. To quantify jaw morphology, we measured two LJ lever systems in approximately 40 species from each lineage. Using geologic calibrations, we generated a chronogram for both groups and examined the rates of jaw evolution in the two radiations. The most rapidly evolving components of the LJ differed between the two radiations. However, the Lake Malawi flock exhibited a much faster rate of evolution in several components of the LJ. This rapid rate of divergence is consistent with natural selection, promoting unparalleled trophic diversification in Lake Malawi cichlids.     

Recent speciation between sympatric Tanganyikan cichlid colour morphs

Lake Tanganyika, Africa's oldest lake, harbours an impressive diversity of cichlid fishes. Although diversification in its radiating groups is thought to have been initially rapid, cichlids from Lake Tanganyika show little evidence for ongoing speciation. In contrast, examples of recent divergence among sympatric colour morphs are well known in haplochromine cichlids from Lakes Malawi and Victoria. Here, we report genetic evidence for recent divergence between two sympatric Tanganyikan cichlid colour morphs. These Petrochromis morphs share mitochondrial haplotypes, yet microsatellite loci reveal that their sympatric populations form distinct genetic groups. Nuclear divergence between the two morphs is equivalent to that which arises geographically within one of the morphs over short distances and is substantially smaller than that among other sympatric species in this genus. These patterns suggest that these morphs diverged only recently, yet that barriers to gene flow exist which prevent extensive admixture despite their sympatric distribution. The morphs studied here provide an unusual example of active diversification in Lake Tanganyika's generally ancient cichlid fauna and enable comparisons of speciation processes between Lake Tanganyika and other African lakes.     

Phylogenomics of pike cichlids (Cichlidae: Crenicichla): the rapid ecological speciation of an incipient species flock

The rapid rise of phenotypic and ecological diversity in independent lake‐dwelling groups of cichlids is emblematic of the East African Great Lakes. In this study, we show that similar ecologically based diversification has occurred in pike cichlids (Crenicichla) throughout the Uruguay River drainage of South America. We collected genomic data from nearly 500 ultraconserved element (UCEs) loci and >260 000 base pairs across 33 species, to obtain a phylogenetic hypothesis for the major species groups and to evaluate the relationships and genetic structure among five closely related, endemic, co‐occurring species (the Uruguay River species flock; URSF). Additionally, we evaluated ecological divergence of the URSF based on body and lower pharyngeal jaw (LPJ) shape and gut contents. Across the genus, we recovered novel relationships among the species groups. We found strong support for the monophyly of the URSF; however, relationships among these species remain problematic, likely because of the rapid and recent evolution of this clade. Clustered co‐ancestry analysis recovered most species as well delimited genetic groups. The URSF species exhibit species‐specific body and LPJ shapes associated with specialized trophic roles. Collectively, our results suggest that the URSF consists of incipient species that arose via ecological speciation associated with the exploration of novel trophic roles.     

Phylogeographic and phenotypic outcomes of brown anole colonization across the Caribbean provide insight into the beginning stages of an adaptive radiation

Some of the most important insights into the ecological and evolutionary processes of diversification and speciation have come from studies of island adaptive radiations, yet relatively little research has examined how these radiations initiate. We suggest that Anolis sagrei is a candidate for understanding the origins of the Caribbean Anolis adaptive radiation and how a colonizing anole species begins to undergo allopatric diversification, phenotypic divergence and, potentially, speciation. We undertook a genomic and morphological analysis of representative populations across the entire native range of A. sagrei, finding that the species originated in the early Pliocene, with the deepest divergence occurring between western and eastern Cuba. Lineages from these two regions subsequently colonized the northern Caribbean. We find that at the broadest scale, populations colonizing areas with fewer closely related competitors tend to evolve larger body size and more lamellae on their toepads. This trend follows expectations for post‐colonization divergence from progenitors and convergence in allopatry, whereby populations freed from competition with close relatives evolve towards common morphological and ecological optima. Taken together, our results show a complex history of ancient and recent Cuban diaspora with populations on competitor‐poor islands evolving away from their ancestral Cuban populations regardless of their phylogenetic relationships, thus providing insight into the original diversification of colonist anoles at the beginning of the radiation. Our research also supplies an evolutionary framework for the many studies of this increasingly important species in ecological and evolutionary research.     

Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika

The spectacularly diverse cichlid fish species flocks of the East African Rift Lakes have elicited much debate on the potential evolutionary mechanisms responsible for the origin of these adaptive radiations. An historical perspective on population structure may offer insights into the processes driving population differentiation and possibly speciation. Here, we examine mitochondrial DNA (mtDNA) sequence variation in two endemic species of rock-dwelling cichlids, Simochromis babaulti and S. diagramma , from Lake Tanganyika. Phylogeographic analyses were used to infer what factors might have been important in the genetic structuring of Simochromis populations. Patterns of mtDNA differentiation in Simochromis were compared to those of other rock-dwelling cichlids to distinguish between competing hypotheses concerning the processes underlying their evolution. In striking contrast to previous findings, populations of Simochromis , even those separated by up to 300 km, were found to share mitochondrial DNA haplotypes. There is no correspondence between mtDNA genealogies and the geographical distribution of populations. Only S. babaulti , but not S. diagramma was found to have a significant association between genetic and geographical distance. These phylogeographic patterns suggest that the evolutionary effects of abiotic and biotic factors shaping population genetic structure may differ substantially even among closely related species of rock-dwelling cichlids. Physical events and barriers to gene flow that are believed to have had a major impact on the geographical distribution and intralacustrine speciation of Tropheus do not seem to have equally strongly affected its close relative Simochromis . These findings emphasize that no single mechanism can be responsible for the formation of population structure, speciation, and the adaptive radiation of all cichlid fishes.     

Molecular investigation of genetic assimilation during the rapid adaptive radiations of East African cichlid fishes

Adaptive radiations are characterized by adaptive diversification intertwined with rapid speciation within a lineage resulting in many ecologically specialized, phenotypically diverse species. It has been proposed that adaptive radiations can originate from ancestral lineages with pronounced phenotypic plasticity in adaptive traits, facilitating ecologically driven phenotypic diversification that is ultimately fixed through genetic assimilation of gene regulatory regions. This study aimed to investigate how phenotypic plasticity is reflected in gene expression patterns in the trophic apparatus of several lineages of East African cichlid fishes, and whether the observed patterns support genetic assimilation. This investigation used a split brood experimental design to compare adaptive plasticity in species from within and outside of adaptive radiations. The plastic response was induced in the crushing pharyngeal jaws through feeding individuals either a hard or soft diet. We find that nonradiating, basal lineages show higher levels of adaptive morphological plasticity than the derived, radiated lineages, suggesting that these differences have become partially genetically fixed during the formation of the adaptive radiations. Two candidate genes that may have undergone genetic assimilation, gif and alas1, were identified, in addition to alterations in the wiring of LPJ patterning networks. Taken together, our results suggest that genetic assimilation may have dampened the inducibility of plasticity related genes during the adaptive radiations of East African cichlids, flattening the reaction norms and canalizing their feeding phenotypes, driving adaptation to progressively more narrow ecological niches.     

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.