Environmental context for understanding the iconic adaptive radiation of cichlid fishes in Lake Malawi

Malinsky, Milan; Salzburger, Walter

doi:10.1073/pnas.1614272113

Cited by 22 publications

(21 citation statements)

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“…By combining our mutation rate with nucleotide diversity (π) values, we estimate the long term effective population sizes (N e ) to be in the range of approximately 50,000 to 130,000 breeding individuals (with N e = π/4µ). Given previous estimates of the age of the radiation of the order of a million years 12,30,31 (max estimate 4.63 million years 32 ), and the hundreds of species present, this result suggests that alleles at a locus will only rarely coalesce within the time between successive speciation events, consistent with high sharing of heterozygosity and ILS. This is because both the mean and standard deviation in the time to the common ancestor of a pair of alleles are expected to be in the order of 2N e generations, or hundreds of thousands of years.…”

Section: Low Per-generation Mutation Ratesupporting

confidence: 62%

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

Malinsky

Svardal

Tyers

et al. 2017

Preprint

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Abstract:The hundreds of cichlid fish species in Lake Malawi constitute the most extensive recent vertebrate adaptive radiation. Here we characterize its genomic diversity by sequencing 134 individuals covering 73 species across all major lineages. Average sequence divergence between species pairs is only 0.1-0.25%. These divergence values overlap diversity within species, with 82% of heterozygosity shared between species. Phylogenetic analyses suggest that diversification initially proceeded by serial branching from a generalist Astatotilapia-like ancestor. However, no single species tree adequately represents all species relationships, with evidence for substantial gene flow at multiple times. Common signatures of selection on visual and oxygen transport genes shared by distantly related deep water species point to both adaptive introgression and independent selection. These findings enhance our understanding of genomic processes underlying rapid species diversification, and provide a platform for future genetic analysis of the Malawi radiation.One Sentence Summary: The genomes of 73 cichlid fish species from Lake Malawi uncover evolutionary processes underlying a large adaptive evolutionary radiation.. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under aThe copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/143859 doi: bioRxiv preprint first posted online May. 31, 2017; Main Text: The formation of every lake or island represents a fresh opportunity for colonization, proliferation and diversification of living forms. In some cases, the ecological opportunities presented by underutilized habitats facilitate adaptive radiation -rapid and extensive diversification of the descendants of the colonizing lineages (1-3). Adaptive radiations are thus exquisite examples of the power of natural selection, as recognized by Darwin in the case of Galapagos finches (4, 5), and seen for example in Anoles lizards of the Caribbean (6) and in East African cichlid fishes (7,8).Cichlids are the most species rich and diverse family of vertebrates, and nowhere are their radiations more spectacular than in the Great Lakes of East Africa: Malawi, Tanganyika, and Victoria (2), each of which contains several hundred endemic species, with the largest number in Lake Malawi. Molecular genetic studies have made major contributions to reconstructing the evolutionary histories of these adaptive radiations, especially in terms of the relationships between the lakes (9), between some major lineages in Lake Tanganyika (10), and in describing the role of hybridization in the origins of the Lake Victoria radiation (11). However, the task of reconstructing within-lake relationships and of identifying sister species in lakes Malawi and Victoria remains challenging due both to retention of large amounts of ancestral genetic polymorphism (i.e. incomplete lineage sorting) and to evidence suggesting gene flow between taxa (12, 13).Initial genome assemblies of cichlids from ...

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Section: Low Per-generation Mutation Ratesupporting

confidence: 62%

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

Malinsky

Svardal

Tyers

et al. 2017

Preprint

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100

172

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“…This three-stage model posits that adaptively radiating clades diverge predictably and sequentially: first along a habitat axis, then along a trophic axis, and finally along a signaling, or sexual trait, axis. The three-stage model has strongly influenced the study of adaptive radiation and has been used to characterize diversity in cichlid lineages ranging from Central America to the East African rift lakes (Salzburger, 2009;Martin and Genner, 2009;Hulsey et al, 2010;Parnell and Streelman, 2011;Kautt et al, 2012;López-Fernández et al, 2012;Hulsey et al, 2013a;Husemann et al, 2014;Muschick et al, 2014;Salzburger et al, 2014;Santos-Santos et al, 2015;Ivory et al, 2016;Malinsky and Salzburger, 2016). This hypothesis of niche evolution has also been invoked as a putative explanation for diversification in a large number of other disparate clades including plants, invertebrates, and other vertebrate groups (Ackerly et al, 2006;Cowman et al, 2009;Harmon et al, 2008;Gavrilets and Losos, 2009;Arnegard et al, 2010;Glor, 2010;Sallan and Friedman, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…For instance, modifications for algivory that is the dominant mode of mbuna feeding or the evolution of specific locomotory abilities associated with navigating complex rocky environments might have led to ecological specialization that was extremely difficult to reverse (Schluter, 2000;Alfaro et al, 2007;Price et al, 2011;Rupp and Hulsey, 2014). Once they initially colonized the rocky reefs in Malawi, the mbuna clade may also have entered a stage in which sexual selection and trophic evolution exclusively drove their diversification (Streelman and Danley, 2003;Malinsky and Salzburger, 2016). Phylogenetic analyses could help to resolve whether major habitat shifts back to sandy habitats have occurred during the mbuna radiation.…”

Section: Introductionmentioning

confidence: 99%

“…Also, if C. obliquidens were well nested within the mbuna radiation, this placement would suggest that following extensive diversification on the rocky outcrops of Lake Malawi, a member of the mbuna clade diverged to exploit sandy habitats. Alternatively, if C. obliquidens were more closely related to non-mbuna living in sandy habitats or was found to be the sister lineage to the 400 species of rock-dwelling mbuna, then it would still be possible that the radiation of mbuna once it evolved to exploit reefs might have remained confined to these rocky habitats (Streelman and Danley, 2003;Malinsky and Salzburger, 2016). Robust phylogenies of Malawi cichlids could be used to test for this extreme niche conservatism and to evaluate through a more complete understanding of Malawi cichlid relationships the strictest interpretation of the three-stage model.…”

Section: Introductionmentioning

confidence: 99%

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Phylogenomic analysis of Lake Malawi cichlid fishes: Further evidence that the three-stage model of diversification does not fit

Hulsey

Zheng

Faircloth

et al. 2017

Molecular Phylogenetics and Evolution

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Adaptive radiations could often occur in discrete stages. For instance, the species flock of ∼1000 species of Lake Malawi cichlid fishes might have only diverged once between rocky and sandy environments during the initial stage of their diversification. All further diversification within the rock-dwelling (mbuna) or sand-dwelling (utaka) cichlids would have occurred during a subsequent second stage of extensive trophic evolution that was followed by a third stage of sexual trait divergence. We provide an improved phylogenetic framework for Malawi cichlids to test this three-stage hypothesis based on newly reconstructed phylogenetic relationships among 32 taxonomically disparate Malawi cichlids species. Using several reconstruction methods and 1037 ultra-conserved element (UCE) markers, we recovered a molecular phylogeny that confidently resolved relationships among most of the Malawi lineages sampled when a bifurcating framework was enforced. These bifurcating reconstructions also indicated that the sand-dwelling species Cyathochromis obliquidens was well-nested within the primarily rock-dwelling radiation known as the mbuna. In contrast to predictions from the three-stage model of vertebrate diversification, the recovered phylogeny reveals an initial colonization of rocky reefs, followed by substantial diversification of rock-dwelling lineages, and then at least one instance of subsequent evolution back into sandy habitats. This repeated evolution into major habitat types provides further evidence that the three-stage model of Malawi cichlid diversification has numerous exceptions.

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“…The approximately 1500 species of African cichlid fishes are a textbook example of adaptive radiations, characterized by phenotypic change in a rapidly speciating lineage (Kocher 2004, Malinsky andSalzburger 2016). Cichlids differ in many extensively studied and ecologically important phenotypes, including examples such as jaw morphology (Albertson et al 2003), color patterns (Seehausen 1996, Danley and Kocher 2001, Allender et al 2003, Konings 2007, sex determination (Roberts et al 2009, Gammerdinger andKocher 2018), and parental care (Barlow 2000, Sefc 2011).…”

Section: Introductionmentioning

confidence: 99%

Movement of transposable elements contributes to cichlid diversity

Carleton

Conte

Malinsky

et al. 2020

Preprint

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African cichlid fishes are a prime model for studying the mechanisms of speciation.Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for variation in cichlid phenotypes. Cichlids have some of the largest known shifts in vertebrate visual sensitivity. These shifts arise mainly from the differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi (LM) cichlids, we have thus far identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or of the opsin gene itself. Here we show that these indels are caused by the movement of transposable elements (TEs). These precise indels are not found outside of LM, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. A similar indel has arisen independently outside of LM at one locus, suggesting that some locations are primed for TE insertion and the resulting indels. Increased TE mobility may be associated with interspecific hybridization, which disrupt mechanisms of TE suppression.Overall, our study suggests that TEs may contribute to key regulatory changes, and may facilitate rapid phenotypic change and possibly speciation in African cichlids.

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Environmental context for understanding the iconic adaptive radiation of cichlid fishes in Lake Malawi

Cited by 22 publications

References 21 publications

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

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

Phylogenomic analysis of Lake Malawi cichlid fishes: Further evidence that the three-stage model of diversification does not fit

Movement of transposable elements contributes to cichlid diversity

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