Genetic basis for divergence in developmental gene expression in two closely related sea urchins

Wang, Lingyu; Israel, Jennifer W.; Edgar, Allison; Raff, Rudolf A.; Raff, Elizabeth C.; Byrne, Maria; Wray, Gregory A.

doi:10.1038/s41559-020-1165-y

Cited by 24 publications

(62 citation statements)

References 58 publications

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“…For example, within Echinoderms, lecithotrophy has independently evolved from the ancestral planktotrophic state more than 20 times (Raff 1987; Wray 1996; McEdward and Miner 2001; Hart 2002), implying that recurring sets of environmental conditions and strong selection can enact evolutionary modifications to even highly conserved developmental processes. The consequences include changes at every developmental stage ranging from egg composition (Prowse, et al 2009; Falkner, et al 2015; Byrne and Sewell 2019; Davidson, et al 2019) and zygotic genome activation (Wray and Raff 1990; Israel, et al 2016; Wang, et al 2020), cell type specification and embryonic patterning (Wray and Raff 1989; Love and Raff 2006), to construction of larval structures such as the skeleton and rudiment (Emlet 1995; Koop, et al 2017), the latter being the region from which the adult emerges during metamorphosis. Still, the impact selection exerts on the evolution of cis -regulatory interactions underlying alternative developmental programs and contrasting life history strategies is not known.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins

Davidson

Byrne

Wray

2022

Preprint

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Chromatin configuration is highly dynamic during embryonic development in animals, exerting an important point of control in transcriptional regulation. Yet there exists remarkably little information about the contribution of evolutionary changes in chromatin configuration to the evolution of gene expression and organismal traits. Genome-wide assays of chromatin configuration, coupled with whole-genome alignments, can help address this gap in knowledge in several ways. In this study we present a comparative analysis of regulatory element sequences and accessibility throughout embryogenesis in three sea urchin species with divergent life histories: a lecithotroph Heliocidaris erythrogramma, a closely related planktotroph H. tuberculata, and a distantly related planktotroph Lytechinus variegatus. We identified distinct epigenetic and mutational signatures of evolutionary modifications to cis-regulatory element function in H. erythrogramma that have accumulated non-uniformly throughout the genome, suggesting selection, rather than drift, underlies many modifications associated with the derived life history. Specifically, regulatory elements composing the sea urchin developmental gene regulatory network are enriched for signatures of positive selection and accessibility changes which may function to alter binding affinity and access of developmental transcription factors to these sites. Furthermore, regulatory element changes often correlate with divergent expression patterns of genes involved in cell type specification, morphogenesis, and development of other derived traits, suggesting these evolutionary modifications have been consequential for phenotypic evolution in H. erythrogramma. Collectively, our results demonstrate that selective pressures imposed by changes in developmental life history rapidly reshape the cis-regulatory landscape of core developmental genes to generate novel traits and embryonic programs.

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Section: Introductionmentioning

confidence: 99%

Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins

Davidson

Byrne

Wray

2022

Preprint

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“…While interspecies comparisons typically focus on only fixed genetic differences between species (McManus et al 2010; Coolon et al 2014), we also included strongly differentiated SNPs in our intraspecies comparison, as fixed sites are relatively rare due to the strong gene flow and differentiated SNPs are also functionally important. Furthermore, our ASE analysis approach simultaneously compares many replicates in a population-level approach (Wang et al 2020) rather than focusing on individual parent-offspring pairs, thus increasing the usefulness of highly differentiated, but non-fixed, SNPs. Subsequently, we remapped all RNA-seq data for hybrid individuals back to the masked reference genome, keeping only uniquely mapping reads, and produced allele-specific haplotype counts for all heterozygous SNPs using the phaser pipeline (Castel et al 2016).…”

Section: Methodsmentioning

confidence: 99%

“…S9). Lastly, to test for allele-specific expression and classify genes by regulatory mode, we followed the statistical approach by Wang et al (Wang et al 2020) based on the criteria by Coolon et al (Coolon et al 2014) (Supplementary text). Compared to Coolon et al (Coolon et al 2014), Wang et al (Wang et al 2020) made use of biological replicates, as we have in our study, and analysed allele-specific expression by fitting Negative binomial generalized linear models and Wald statistical tests using DESeq2 .…”

Section: Methodsmentioning

confidence: 99%

“…Lastly, to test for allele-specific expression and classify genes by regulatory mode, we followed the statistical approach by Wang et al (Wang et al 2020) based on the criteria by Coolon et al (Coolon et al 2014) (Supplementary text). Compared to Coolon et al (Coolon et al 2014), Wang et al (Wang et al 2020) made use of biological replicates, as we have in our study, and analysed allele-specific expression by fitting Negative binomial generalized linear models and Wald statistical tests using DESeq2 . In brief, we compared NY/GA alleles in hybrids using the transTest with the following formula design: ‘∼0 + Gen * Origin’, with ‘Gen’ denoting the allele (GA or NY) in hybrids and ‘Origin’ denoting whether reads were from the parental individuals or hybrids.…”

Section: Methodsmentioning

confidence: 99%

“…To reduce the impact of allele-specific mapping bias on our analyses, we first produced a reference genome with all fixed and nearly fixed SNPs between populations masked. We did this by first calling SNPs from the genome-aligned RNA-seq data using GATK v. Furthermore, our ASE analysis approach simultaneously compares many replicates in a population-level approach (Wang et al 2020) rather than focusing on individual parentoffspring pairs, thus increasing the usefulness of highly differentiated, but non-fixed, SNPs.…”

Section: Limitations Andmentioning

confidence: 99%

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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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Extreme phenotypic divergence and the evolution of development

Wray¹

2022

Current Topics in Developmental Biology

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Genetic basis for divergence in developmental gene expression in two closely related sea urchins

Cited by 24 publications

References 58 publications

Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins

Evolutionary changes in the chromatin landscape contribute to reorganization of a developmental gene network during rapid life history evolution in sea urchins

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

Extreme phenotypic divergence and the evolution of development

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