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The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes.

ABSTRACT: Adaptive radiation research typically relies on the study of evolution in retrospective, leaving the predictive value of the concept hard to evaluate. Several radiations, including the cichlid fishes in the East African Great Lakes, have been studied extensively, yet no study has investigated the onset of the intraspecific processes of niche expansion and differentiation shortly after colonization of an adaptive zone by cichlids. Haplochromine cichlids of one of the two lineages that seeded the Lake Victoria radiation recently arrived in Lake Chala, a lake perfectly suited for within-lake cichlid speciation. Here, we infer the colonization and demographic history, quantify phenotypic, ecological and genomic diversity and diversification, and investigate the selection regime to ask if the population shows signs of diversification resembling the onset of adaptive radiation. We find that since their arrival in the lake, haplochromines have colonized a wide range of depth habitats associated with ecological and morphological expansion and the beginning of phenotypic differentiation and potentially nascent speciation, consistent with the very early onset of an adaptive radiation process. Moreover, we demonstrate evidence of rugged phenotypic fitness surfaces, indicating that current ecological selection may contribute to the phenotypic diversification.

SUBMITTER: Moser FN

PROVIDER: S-EPMC6111161 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes.

Moser Florian N FN van Rijssel Jacco C JC Mwaiko Salome S Meier Joana I JI Ngatunga Benjamin B Seehausen Ole O

Proceedings. Biological sciences 20180815 1884

Adaptive radiation research typically relies on the study of evolution in retrospective, leaving the predictive value of the concept hard to evaluate. Several radiations, including the cichlid fishes in the East African Great Lakes, have been studied extensively, yet no study has investigated the onset of the intraspecific processes of niche expansion and differentiation shortly after colonization of an adaptive zone by cichlids. Haplochromine cichlids of one of the two lineages that seeded the ...[more]

PMID: 30111604

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Project description:BackgroundAfter a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (approximately 20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation.ResultsGene coalescence analyses [11 microsatellite loci and mitochondrial DNA (mtDNA) sequences] suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thin- and thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (delta15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thin- and thick-lipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001).ConclusionsThis study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification.

Project description:BackgroundUnderstanding 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 findingsHere 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/significanceOur 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.

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The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes.

Publications

The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes.

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