cis-Regulatory changes in locomotor genes are associated with the evolution of burrowing behavior

Hu, Caroline; York, Ryan A.; Metz, Hillery C; Bedford, Nicole L.; Fraser, Hunter B.; Hoekstra, Hopi E.

doi:10.1016/j.celrep.2022.110360

Cited by 23 publications

(15 citation statements)

References 45 publications

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“…Interestingly, we found that genes with evidence for tissue-specific ASE in particular were enriched in regions of recurrent marine-freshwater divergence. Tissue- or context-specific cis -regulatory differences have previously been shown to underlie adaptive traits in sticklebacks [4,14] and other systems[40]. The tissue- and developmental-specificity of cis -regulatory changes we identified between marine and freshwater sticklebacks highlights the utility of studying gene regulation across multiple tissues and contexts in understanding regulatory adaptation.…”

Section: Discussionmentioning

confidence: 74%

Evolution of spatial and temporalcis-regulatory divergence between marine and freshwater sticklebacks

Mack

Square

Zhao

et al. 2022

Preprint

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Cis-regulatory changes are thought to play a major role in adaptation. Threespine sticklebacks have repeatedly colonized freshwater habitats in the Northern Hemisphere, where they have evolved a suite of phenotypes that distinguish them from marine populations, including changes in physiology, behavior, and morphology. To understand the role of gene regulatory evolution in adaptive divergence, here we investigate cis-regulatory changes in gene expression between marine and freshwater ecotypes through allele-specific expression (ASE) in F1 hybrids. Surveying seven ecologically relevant tissues, including three sampled across two developmental stages, we identified cis-regulatory divergence affecting a third of genes, nearly half of which were tissue-specific. Next, we compared allele-specific expression in dental tissues at two timepoints to characterize cis-regulatory changes during development between marine and freshwater fish. Applying a genome-wide test for selection on cis-regulatory changes, we find evidence for lineage-specific selection on several processes, including the Wnt signaling pathway in dental tissues. Finally, we show that genes with ASE, particularly those that are tissue-specific, are enriched in genomic regions associated with marine-freshwater divergence, supporting an important role for cis-regulatory differences in adaptive evolution of sticklebacks. Altogether, our results provide insight into the cis-regulatory landscape of divergence between stickleback ecotypes and supports a fundamental role for cis-regulatory changes in rapid adaptation to new environments.

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Section: Discussionmentioning

confidence: 74%

Evolution of spatial and temporalcis-regulatory divergence between marine and freshwater sticklebacks

Mack

Square

Zhao

et al. 2022

Preprint

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“…In hybrids, the genomes of both species share the same nucleus and are exposed to identical environments, so there are no confounding environmental, batch, compositional, or developmental effects. This approach has been successfully applied in many species and advanced our understanding of the evolution of gene regulation and its role in establishing phenotypic variation (Hu et al 2022; Mack, Campbell, and Nachman 2016; Combs et al 2018; X. Zhang and Borevitz 2009).…”

Section: Introductionmentioning

confidence: 99%

“…In hybrids, the genomes of both species share the same nucleus and are exposed to identical environments, so there are no confounding environmental, batch, compositional, or developmental effects. This approach has been successfully applied in many species and advanced our understanding of the evolution of gene regulation and its role in establishing phenotypic variation [10][11][12][13]. Furthermore, the recent development of human-chimpanzee allotetraploid "hybrid" cells and organoids enables detailed, accurate quantification of differences in gene expression between humans and our closest living relatives [8,9,14].…”

Section: Introductionmentioning

confidence: 99%

Accounting for cis-regulatory constraint prioritizes genes likely to affect species-specific traits

Starr

Gokhman

Fraser

2022

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Measuring differences in allele specific gene expression in hybrids between two different species is a powerful way to detect cis-regulatory changes underlying adaptation. However, these studies frequently identify thousands of differentially expressed genes. This makes it difficult to differentiate candidate genes most likely to explain interspecies phenotypic differences from genes whose expression levels diverge with little evolutionary constraint. Here we outline a simple strategy that leverages population-scale allele-specific RNA-seq data to identify genes that have constrained cis-regulation within species yet show divergence between species. By applying this strategy to data from human/chimpanzee hybrid cortical spheroids we identify signatures of lineage-specific selection on the expression of genes related to cellular proliferation, speech, glucose metabolism, and glycan degradation. In addition, we highlight human-derived differences in the expression of CUX1 and EDNRB that may contribute to differences in neural connectivity and brain size between humans and other primates.

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“…In particular, incompatible regulatory alleles might accumulate between non-recombining inversion-linked haplotypes (Berdan et al 2021). However, gene regulatory mechanisms can be highly context-dependent, meaning that gene regulatory variation and/or incompatibilities, and hence inversions, might only act and become visible in specific environments, tissues, sexes and/or life-stages (York et al 2018; Mugal et al 2020; Berdan et al 2021; Hu et al 2022). It remains unclear, if such regulatory incompatibilities and associated hybrid misexpression can arise under ongoing pervasive gene flow, and if so, how this is facilitated by tightly-linked genomic architectures.…”

Section: Introductionmentioning

confidence: 99%

Temperature-dependent gene regulatory divergence underlies local adaptation with gene flow in the Atlantic silverside

Jacobs

Velotta

Tigano

et al. 2022

Preprint

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Gene regulatory divergence is thought to play an important role in adaptation, yet its extent and underlying mechanisms remain largely elusive under scenarios of local adaptation with gene flow. Local adaptation is widespread in marine species despite generally high connectivity and often associated with tightly-linked genomic architectures, such as chromosomal inversions. To investigate gene regulatory evolution under gene flow and the role of discrete genomic regions associated with local adaptation to a steep thermal gradient, we generated RNA-seq data from Atlantic silversides (Menidia menidia) from two locally adapted populations and their F1 hybrids, reared under two different temperatures. We found substantial divergence in gene expression and thermal plasticity, with up to 31% of genes being differentially expressed, and primarily trans-rather than cis-regulatory divergence between populations, despite ongoing gene flow. Substantially reduced thermal plasticity, temperature-dependent gene misexpression and the disruption of co-expression networks in hybrids point toward a role of regulatory incompatibilities in maintaining local adaptation, particularly under colder temperatures, which appear more challenging for this species. Adaptive chromosomal inversions seem to play an important role in gene regulatory divergence through the accumulation of regulatory incompatibilities but are not consistently enriched for divergently regulated genes. Together, these results highlight that gene regulation can diverge substantially among populations connected by strong gene flow in marine environments, partly due to the accumulation of temperature-dependent regulatory incompatibilities within inversions.

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cis-Regulatory changes in locomotor genes are associated with the evolution of burrowing behavior

Cited by 23 publications

References 45 publications

Evolution of spatial and temporalcis-regulatory divergence between marine and freshwater sticklebacks

Evolution of spatial and temporalcis-regulatory divergence between marine and freshwater sticklebacks

Accounting for cis-regulatory constraint prioritizes genes likely to affect species-specific traits

Temperature-dependent gene regulatory divergence underlies local adaptation with gene flow in the Atlantic silverside

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