Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes

Carruthers, Madeleine; Edgley, Duncan E.; Saxon, Andrew D.; Gabagambi, Nestory P.; Shechonge, Asilatu; Miska, Eric A.; Durbin, Richard; Bridle, Jon R.; Turner, George F.; Genner, Martin J.

doi:10.1093/molbev/msac251

Cited by 13 publications

(20 citation statements)

References 112 publications

(223 reference statements)

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“…Given ecotype divergence at many – at least a hundred or so – genomic loci (Malinsky et al 2015), we could expect that recombination, or the lack thereof, would be important in bringing together and keeping together the alleles that are beneficial in each environment (Ortiz-Barrientos et al 2016; Todesco et al 2020; Schluter and Rieseberg 2022; Battlay et al 2023). Our findings reveal and characterize substantial differences in population recombination rates between the ecotypes, complementing previous studies of divergence in ecology, mate choice, and allele frequencies (Malinsky et al 2015), methylation (Vernaz et al 2022), gene expression (Carruthers et al 2022), and in sex determination (Munby et al 2021).…”

Section: Discussionsupporting

confidence: 84%

Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Talbi,

Turner,

Malinsky

2024

Preprint

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Meiotic recombination is fundamental to evolution of sexually reproducing organisms and differences in recombination rates are important during rapid adaptation and organismal diversification. Many unknowns remain regarding how and why recombination landscapes evolve in nature. Here, we reconstruct recombination maps based on linkage disequilibrium and use subsampling and simulations to show that fine-scale recombination landscapes differ substantially between two cichlid fish ecotypes ofAstatotilapia callipterathat diverged only ∼2,500 generations ago. The observed results are not driven by PDRM9, whose binding sites do not show any relationship to recombination rates in this species. We show that regions where recombination histories differ between ecotypes have non-random distribution across chromosomes. They are associated with, but only partially explained, by regions of high divergence between ecotypes in allele frequency (FST) and / or nucleotide diversity. We also found 47 large haplotype blocks that are polymorphic in Lake Masoko, cover 21% of the genome, appear to include inversions, and contribute disproportionately to the evolution of recombination. Only a small number of them have elevatedFST. While some haplotype blocks are old and likely maintained by balancing selection, for most, the age of ancestry is close to the genome-wide average. Among haplotype blocks, there is a strong and clear association between the degree of recombination divergence and ecotype clustering by individual heterozygosity. Overall, our work provides a holistic view of changes in recombination landscapes during early stages of speciation with gene flow and advances our understanding of the combinatorial basis of evolution.

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Section: Discussionsupporting

confidence: 84%

Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Talbi,

Turner,

Malinsky

2024

Preprint

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“…The impact of post-transcriptional processing on adaptation is a small but growing field of research. Many previous studies have focused on a particular phenotype associated with alternative splicing in a single gene (Gacheva et al 2011;Jarosch et al 2011;Howes et al 2017;Ceinos et al 2018). In contrast, we looked for signatures of adaptive, alternative splicing genome-wide.…”

Section: Discussionmentioning

confidence: 99%

“…Heritable variation in gene expression is a well-known source of adaptive evolution but has been primarily studied in the context of transcript abundance. Nonetheless, there is an increasing recognition of the importance of post-transcriptional regulation, and a handful of studies have used genome-wide short-read RNA-Seq to study mRNA abundance in conjunction with alternative splicing in the context of local adaptation (Huang et al 2021;Jacobs & Elmers 2021;Carruthers et al 2022;Singh et al 2022;Steward et al 2022;Huang et al 2023). Several patterns have emerged from these studies.…”

Section: Discussionmentioning

confidence: 99%

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Alternative splicing and environmental adaptation in house mice

Manahan,

Nachman

2023

Preprint

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A major goal of evolutionary genetics is to understand the genetic and molecular mechanisms underlying adaptation. Previous work has established that changes in gene regulation may contribute to adaptive evolution, but most studies have focused on mRNA abundance and only a few studies have investigated the role of post-transcriptional processing. Here, we use a combination of exome sequences and short-read RNA-Seq data from wild house mice (Mus musculus domesticus) collected along a latitudinal transect in eastern North America to identify candidate genes for local adaptation through alternative splicing. First, we identified alternatively spliced transcripts that differ in frequency between mice from the northern-most and southern-most populations in this transect. We then identified the subset of these transcripts that exhibit clinal patterns of variation among all populations in the transect. Finally, we conducted association studies to identifycis-acting splicing quantitative trait loci (cis-sQTL), and we identifiedcis-sQTL that overlapped with previously ascertained targets of selection from genome scans. Together, these analyses identified a small set of alternatively spliced transcripts that may underlie environmental adaptation in house mice. Many of these genes have known phenotypes associated with body size, a trait that varies clinally in these populations. We observed no overlap between these genes and genes previously identified by changes in transcript level, indicating that alternative splicing and changes in mRNA abundance may provide separate molecular mechanisms of adaptation.

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“…Gene expression plays an important role in ecological speciation and can be an early indicator of species divergence (Wolf et al., 2010). Divergence in gene expression can contribute to hybrid speciation via niche specialization, reproductive isolation from parent species or both (Carruthers et al., 2022; Pavey et al., 2010; Renaut et al., 2009). It has also been suggested that gene expression plasticity could be important for species to adapt to climate change (Kelly, 2019), however climate imposed selection can potentially reduce that plasticity (Kelly et al., 2017).…”

Section: Introductionmentioning

confidence: 99%

Transgressive gene expression and expression plasticity under thermal stress in a stable hybrid zone

Schwartz,

González,

Strong

et al. 2024

Molecular Ecology

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Interspecific hybridization can lead to myriad outcomes, including transgressive phenotypes in which the hybrids are more fit than either parent species. Such hybrids may display important traits in the context of climate change, able to respond to novel environmental conditions not previously experienced by the parent populations. While this has been evaluated in an agricultural context, the role of transgressive hybrids under changing conditions in the wild remains largely unexplored; this is especially true regarding transgressive gene expression. Using the blue mussel species complex (genus Mytilus) as a model system, we investigated the effects of hybridization on temperature induced gene expression plasticity by comparing expression profiles in parental species and their hybrids following a 2‐week thermal challenge. Hybrid expression plasticity was most often like one parent or the other (50%). However, a large fraction of genes (26%) showed transgressive expression plasticity (i.e. the change in gene expression was either greater or lesser than that of both parent species), while only 2% were intermediately plastic in hybrids. Despite their close phylogenetic relationship, there was limited overlap in the differentially expressed genes responding to temperature, indicating interspecific differences in the responses to high temperature in which responses from hybrids are distinct from both parent species. We also identified differentially expressed long non‐coding RNAs (lncRNAs), which we suggest may contribute to species‐specific differences in thermal tolerance. Our findings provide important insight into the impact of hybridization on gene expression under warming. We propose transgressive hybrids may play an important role in population persistence under future warming conditions.

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Ecological Speciation Promoted by Divergent Regulation of Functional Genes Within African Cichlid Fishes

Cited by 13 publications

References 112 publications

Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Alternative splicing and environmental adaptation in house mice

Transgressive gene expression and expression plasticity under thermal stress in a stable hybrid zone

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