Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Vernaz, Grégoire; Malinsky, Milan; Svardal, Hannes; Du, Mingliu; Tyers, Alexandra M.; Santos, M. Emília; Durbin, Richard; Genner, Martin J.; Turner, George F.; Miska, Eric A.

doi:10.1101/2020.11.24.383034

Cited by 8 publications

(21 citation statements)

References 83 publications

(180 reference statements)

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“…This potential link between the evolution of three-node motifs as part of GRNs associated with cichlid adaptive traits requires further experimental verification. This is beyond that described for cis-regulatory sites previously 44 , as well as support based on large-scale genotyping 41,42,55 and transcriptome evolution 60 ; epigenetic divergence 39,62 ; transgenesis assays 8,58 ; population studies and CRISPR mutant assays 37 ; and transcriptomic/cis-regulatory assays 23,45,46,57 of cichlid species.…”

Section: Discussionmentioning

confidence: 77%

Evolution of miRNA binding sites and regulatory networks in cichlids

Mehta

Penso-Dolfin

Nash

et al. 2021

Preprint

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The divergence of regulatory regions and gene regulatory network (GRN) rewiring is a key driver of cichlid phenotypic diversity. However, the contribution of miRNA binding site turnover has yet to be linked to GRN evolution across cichlids. Here, we extend our previous studies by analysing the selective constraints driving evolution of miRNA and transcription factor (TF) binding sites of target genes, to infer instances of cichlid GRN rewiring associated with regulatory binding site turnover. Comparative analyses identified increased species-specific networks that are functionally associated to traits of cichlid phenotypic diversity. The evolutionary rewiring is associated with differential models of miRNA and TF binding site turnover, driven by a high proportion of fast-evolving polymorphic sites in adaptive trait genes compared to subsets of random genes. Positive selection acting upon discrete mutations in these regulatory regions is likely to be an important mechanism in rewiring GRNs in rapidly radiating cichlids. Regulatory variants of functionally associated miRNA and TF binding sites of visual opsin genes differentially segregate according to phylogeny and ecology of Lake Malawi species, identifying both rewired e.g. clade-specific and conserved network motifs of adaptive trait associated GRNs. Our approach revealed several novel candidate regulators, regulatory regions and three-node motifs across cichlid genomes with previously reported associations to known adaptive evolutionary traits.

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Section: Discussionmentioning

confidence: 77%

Evolution of miRNA binding sites and regulatory networks in cichlids

Mehta

Penso-Dolfin

Nash

et al. 2021

Preprint

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“…Notably, methylome divergence in developmental genes has been shown previously to account for close to half of all species-specific epigenetic differences between three species of the Lake Malawi cichlid radiation (7).…”

Section: Population-specific Methylome Divergence During Early Stages Of Speciationmentioning

confidence: 91%

“…The genomic basis of adaptive phenotypic diversification and speciation has been extensively studied but many questions remain (1-3). Recent studies in plants and animals have provided initial evidence for a contribution of heritable epigenetic divergence to functional phenotypic traits (4)(5)(6)(7)(8)(9). However, whether epigenetic processes facilitate adaptive diversification, especially during the early stages of speciation, remains unknown.…”

Section: Main Textmentioning

confidence: 99%

“…3B). Fixed DMRs might represent population-specific tissueindependent methylome patterns, possibly reflecting distinct core developmental processes (7). Examples of genes with functions during brain development and neuron morphogenesis and showing fixed populationspecific methylome patterns include the embryonic transcription regulator SMAD family member 4a (smad4a; hypomethylated in littorals only) and the scaffolding protein tanc2 (hypomethylated in benthics) (Fig.…”

Section: Plasticity and Inheritance Of Population-specific Methylome Divergencementioning

confidence: 99%

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Epigenetic Divergence during Early Stages of Speciation in an African Crater Lake Cichlid Fish

Vernaz

Hudson

Santos

et al. 2021

Preprint

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Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here we assess the epigenetic basis of diversification during the early stages of speciation. We focus on the extent and functional relevance of DNA methylome divergence between two Astatotilapia calliptera ecomorphs in crater Lake Masoko, southern Tanzania. We report extensive genome-wide methylome divergence between populations linked to key biological processes, including transcriptional activity of ecologically-relevant genes. These include genes involved in steroid metabolism, haemoglobin composition and erythropoiesis, consistent with divergent habitat occupancy of the ecomorphs. Using a common garden experiment, we found that global methylation profiles are rapidly remodelled across generations, but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to early stages of vertebrate speciation.

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“…Plastic phenotypic differentiation through epigenetic changes can be the first stage in adaptation to changing environmental conditions (Hu et al, 2021; Mäkinen et al, 2018), although the overall importance of this mechanism is still unclear. However, Vernaz et al (2021) found substantial DNA methylation differentiation, associated with changes in transcriptome activity of ecologically relevant genes, among sympatric Lake Malawi cichlid species, in spite of their low DNA sequence differentiation. Campbell et al (2021) compared Arctic charr reared at 9°C and 5°C and found significant differences in craniofacial morphology and vertebral number.…”

Section: Evolution Of Salmonid Sympatric Populationsmentioning

confidence: 99%

Identifying and conserving sympatric diversity in trout of the genus Salmo, with particular reference to Lough Melvin, Ireland

Ferguson

Prodöhl

2022

Ecology of Freshwater Fish

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Salmonid (Salmonidae) sympatric diversity is the co-occurrence, in a lake or river, of two or more reproductively isolated populations/subpopulations, or phenotypes resulting from phenotypic plasticity. Sympatric populations can arise through allopatric and/ or sympatric evolution. Subsequently, allopatric lineages can occur in sympatry due to independent colonisation and/or through anthropogenic introduction. Sympatric divergence is often driven by feeding opportunities, with populations segregating as planktivorous, benthivorous and piscivorous ecotypes ("trophic polymorphism"), and further segregation occurring by feeding depth and body size. Subpopulations evolve by natal homing where a water has two or more discrete spawning areas, often resulting in phenotypically and ecologically cryptic sympatry. Most known sympatric populations/phenotypes in trout of the genus Salmo (Eurasian trout aka brown trout) involve sympatric piscivorous (ferox) and lifetime invertivorous trout. Segregation on the benthic-limnetic axis has been poorly studied in Eurasian trout compared with other salmonids but is likely commoner than currently described. While three sympatric populations/species of Eurasian trout are recognised from Lake Ohrid (Albania/ North Macedonia), limited ecological information is available and there are only two lakes with three or four sympatric populations with described benthic, limnetic and piscivorous trophic segregation: Lough Melvin (Ireland) and Loch Laidon (Scotland), the latter having the only identified case of a sympatric profundal benthic feeding populations, possibly due to the absence of Arctic charr (Salvelinus alpinus) in the lake.Many thousands of waters are yet to be examined. Some sympatric populations are extinct, and others are vulnerable with conservation action being urgently required. This should ideally be based on populations/conservation units, but the lack of recognition of intraspecific units in most legislations in the native Eurasian trout range necessitates a pragmatic approach, with species classification, where appropriate, based on integrative taxonomy. Some sympatric populations clearly merit species status and should be formally classified as such if a valid previous name is not available.

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Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes

Cited by 8 publications

References 83 publications

Evolution of miRNA binding sites and regulatory networks in cichlids

Evolution of miRNA binding sites and regulatory networks in cichlids

Epigenetic Divergence during Early Stages of Speciation in an African Crater Lake Cichlid Fish

Identifying and conserving sympatric diversity in trout of the genus Salmo, with particular reference to Lough Melvin, Ireland

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