Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow

Malinsky, Milan; Svardal, Hannes; Tyers, Alexandra M.; Miska, Eric A.; Genner, Martin J.; Turner, George F.; Durbin, Richard

doi:10.1038/s41559-018-0717-x

Cited by 441 publications

(616 citation statements)

References 106 publications

(159 reference statements)

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“…Recently diverged species share genetic polymorphisms due to their common ancestry (incomplete lineage sorting [ILS]) and are often characterized by “porous” genomes that are open to gene flow during ongoing or secondary contact (Malinsky, Svardal, et al, ; Mallet, Besansky, & Hahn, ; Rheindt & Edwards, ; Seehausen, ). This shared variation can make it difficult to detect subtle patterns of population structure.…”

Section: Introductionmentioning

confidence: 99%

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

et al. 2019

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Recently evolved species typically share genetic variation across their genomes due to incomplete lineage sorting and/or ongoing gene flow. Given only subtle allele frequency differences at most loci and the expectation that divergent selection may affect only a tiny fraction of the genome, distinguishing closely related species based on multi‐locus data requires substantial genomic coverage. In this study, we used ddRAD‐seq to sample the genomes of five recently diverged, New World “mallards” (Anas spp.), a group of dabbling duck species characterized by diagnosable phenotypic differences but minimal genetic differentiation. With increased genomic sampling, we aimed to characterize population structure within this group and identify genomic regions that may have experienced divergent selection during speciation. We analyzed 3,017 autosomal ddRAD‐seq loci and 177 loci from the Z‐chromosome. In contrast to previous studies, the ddRAD‐seq data were sufficient to assign individuals to their respective species or subspecies and to generate estimates of gene flow in a phylogenetic framework. We find limited evidence of contemporary gene flow between the dichromatic mallard and several monochromatic taxa, but find evidence for historical gene flow between some monochromatic species pairs. We conclude that the overall genetic similarity of these taxa likely reflects retained ancestral polymorphism rather than recent and extensive gene flow. Thus, despite recurring cases of hybridization in this group, our results challenge the current dogma predicting the genetic extinction of the New World monochromatic dabbling ducks via introgressive hybridization with mallards. Moreover, ddRAD‐seq data were sufficient to identify previously unknown outlier regions across the Z‐chromosome and several autosomal chromosomes that may have been involved in the diversification of species in this recent radiation.

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Section: Introductionmentioning

confidence: 99%

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

et al. 2019

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“…Cichlid fishes are one of the most diverse teleost families and well‐known for their ability to rapidly diversify into various ecological niches through adaptations to a wide range habitats and with respect to different depth ranges, food sources and/or feeding modes (Brawand et al, ; Salzburger, ). Cichlid fishes, and in particular the exceptionally species‐rich cichlid assemblages in the East African Great Lakes Victoria, Malawi and Tanganyika, are also well‐known as classic models for adaptive radiation (Malinsky et al, ; Muschick, Indermaur, & Salzburger, ; Seehausen, ; Verheyen, Salzburger, Snoeks, & Meyer, ). Less species‐rich cichlid assemblages have been reported from various water bodies, for example from small crater lakes in Africa (Malinsky et al, ; Schliewen, Tautz, & Paabo, ) or Nicaragua (Barluenga, Stölting, Salzburger, Muschick, & Meyer, ; Kautt, Elmer, & Meyer, ), permitting important insights into the early phases of incipient speciation.…”

Section: Introductionmentioning

confidence: 99%

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

et al. 2019

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In deep‐water animals, the visual sensory system is often challenged by the dim‐light environment. Here, we focus on the molecular mechanisms involved in rapid deep‐water adaptations. We examined visual system evolution in a small‐scale yet phenotypically and ecologically diverse adaptive radiation, the species flock of cichlid fishes in deep crater lake Barombi Mbo in Cameroon, West Africa. We show that rapid adaptations of the visual system to the novel deep‐water habitat primarily occurred at the level of gene expression changes rather than through nucleotide mutations, which is compatible with the young age of the radiation. Based on retinal bulk RNA sequencing of all eleven species, we found that the opsin gene expression pattern was substantially different for the deep‐water species. The nine shallow‐water species feature an opsin palette dominated by the red‐sensitive (LWS) opsin, whereas the two unrelated deep‐water species lack expression of LWS and the violet‐sensitive (SWS2B) opsin, thereby shifting the cone sensitivity to the centre of the light spectrum. Deep‐water species further predominantly express the green‐sensitive RH2Aα over RH2Aβ. We identified one amino acid substitution in the RH2Aα opsin specific to the deep‐water species. We finally performed a comparative gene expression analysis in retinal tissue of deep‐ vs. shallow‐water species. We thus identified 46 differentially expressed genes, many of which are associated with functions in vision, hypoxia management or circadian clock regulation, with some of them being associated with human eye diseases.

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“…Cichlids from the African great lakes are a unique system in the sense that they represent a large assemblage of closely related, often sympatric species evolving under nonnegligible levels of gene flow, which poses well‐known difficulties for species identification and for the assessment of their evolutionary history (Loh et al, ; Malinsky et al, ; Salzburger, ). However, the results of our study are potentially relevant for other biological systems where the number of real clusters is unknown and/or the sample sizes are naturally unbalanced.…”

Section: Resultsmentioning

confidence: 99%

A population genetic assessment of taxonomic species: The case of Lake Malawi cichlid fishes

Pinho

Cardoso

Hey

2019

Molecular Ecology Resources

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The processes of discovering new species and of assigning individuals to previously described species sometimes come into conflict with the concept of a species as a sexual evolving lineage. For example, species diagnosis and species identification, by human investigators, frequently depend upon the use of diagnostic characters (Cracraft, 1983), but diagnostic characters per se play no role in the theory of how species come into being or how they persist. Species do of course evolve derived fixed traits that sometimes serve well as diagnostic characters, but cryptic species are also common (Bickford et al., 2007). For species that are highly visual, and for which coloration

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Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow

Cited by 441 publications

References 106 publications

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon

A population genetic assessment of taxonomic species: The case of Lake Malawi cichlid fishes

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