Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies

McGirr, Joseph A.; Martin, Christopher H.

doi:10.1002/evl3.41

Cited by 32 publications

(59 citation statements)

References 76 publications

(194 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…4A,C; 95% HPD sweep ages: 6,747-8,490 and 6,594-9,210 years, respectively). Cfap20 and prlh were also both differentially expressed between trophic specialists at early developmental stages, consistent with a cis -regulatory function of these variants (Data S4-S5;( 21 )).…”

Section: Main Textsupporting

confidence: 69%

See 1 more Smart Citation

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

Richards

McGirr²,

Wang³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed 17 the spatial and temporal histories of genetic variants underlying major phenotypic axes of 18 diversification from the genomes of 202 Caribbean pupfishes. Ancient standing variation from 19 disparate spatial sources was reassembled into new combinations which are under strong 20 selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. 21 This occurred in three stages: first, standing variation associated with feeding behavior swept, 22 103 7 which scale-eater candidate adaptive variants were significantly enriched, with relevant terms 104 corresponding to major axes of divergence in this radiation highlighted in bold (FDR < 0.01; full 105 list of terms with FDR < 0.05 in Table S4). 106 107 Even though both trophic specialists are endemic to SSI, we also found nearly all their 108 candidate adaptive variants to occur as standing genetic variation across the Caribbean 109 (molluscivore: 100%; scale-eater: 98%; Fig. 2A). Furthermore, nearly half these variants were 110 ancient and also found in Cualac or Megupsilon outgroups to Cyprinodon (41% and 55% of 111 scale-eater and molluscivore adaptive variants, respectively), which diverged over 5 Mya (22). 112 However, most adaptive variants did not show any evidence of selection in five other focal high- 113 coverage Caribbean generalist populations (only 2% and 6% of scale-eater and molluscivore 114 variants, respectively; Fig. S3) and strong linkage disequilibrium among adaptive variants in SSI 115 trophic specialists was not observed in these focal populations (Fig. 2B). Thus, novel trophic 116 specialists within a microendemic adaptive radiation were almost entirely assembled from 117 ancient standing genetic variation through strong selection for new adaptive combinations of 118 alleles. 119 Multiple lines of evidence suggest that more hybridization and adaptive introgression 120 took place in SSI populations than other Caribbean island populations, consistent with the 121 hypothesis that hybridization triggered adaptive radiation. First, the strongest signal of 122 introgression across the Caribbean was into the root node of the SSI radiation (Fig. 3B). Second, 123 trophic specialists on San Salvador experienced at least twice as much adaptive introgression as 124 other generalist populations across the Caribbean (P < 0.006; Fig. 3C). Third, based on 125 129 9 130 Fig. 3. A history of hybridization across the Caribbean. A) A summary map of adaptive 131 introgression into SSI trophic specialists from focal generalist populations across the Caribbean, 132 with thickness of arrows proportional to the number of outlier regions of the fd statistic. B) 133 149 (mediated through foraging behavior: scale-eating or snail-eating), trophic morphology, and 150 sexual communication signals. Based on both GO annotations of genes near candidate adaptive 151 variants and genome-wide association mapping (GWAS) in Caribbean pupfishes for ...

show abstract

Section: Main Textsupporting

confidence: 69%

“…2C; Table S4). 45% of these genes were also differentially expressed between trophic specialists (FDR < 0.05; Data S4-S5) in whole embryos at 2 and/or 8 days post fertilization (dpf) ( 21 ).…”

Section: Main Textmentioning

confidence: 99%

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

Richards

McGirr²,

Wang³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Parallelism in gene expression using whole transcriptome sequencing has been extensively studied in animals, in insects (Reed et al, 2011; Zhao et al, 2015) and fish species (Derome & Bernatchez, 2006; McGirr & Martin, 2018) in particular. In turn, such studies in plants remain scarce and generally focused only on expression patterns of particular genes or metabolic pathways (Chen et al, 2014; Des Marais & Rausher, 2010; Streisfeld & Rausher, 2009).…”

Section: Introductionmentioning

confidence: 99%

Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa

Wos

Bohutínská

Nosková

et al. 2020

Preprint

View full text Add to dashboard Cite

27Parallel adaptation results from independent evolution of similar traits between closely related 28 lineages and allows testing to which extent evolution is repeatable. Parallel adaptation often 29 involves similar gene expression changes but the identity of genes shaped by parallel selection 30 and the causes of expression parallelism remains largely unknown. By comparing genomes 31 and transcriptomes of four independent foothill-alpine population pairs across four 32 treatments, we addressed genetic basis, plasticity and functional consequences of gene 33 expression parallelism in alpine adaptation. Seeds of four population pairs of Arabidopsis 34 arenosa from distinct mountain regions were raised under four treatments that differed in 35 temperature and irradiance, factors varying strongly with elevation. Parallelism in gene 36 expression was quantified by RNA-seq in leaves of young plants. By manipulating 37temperature and irradiance, we also tested for parallelism in plasticity (gene-by-environment 38 interaction [GEI]). We found significant parallelism in differential gene expression across 39 four independently recruited alpine ecotypes with an overrepresentation of genes involved in 40 biotic stress response. In addition, we demonstrated significant parallelism in GEI indicating 41 shared response to environmental variation in our foothill and alpine populations. Fraction of 42 genes showing expression parallelism also encompassed genomic variants showing outlying 43 differentiation, with greater enrichment of such variants in cis-regulatory elements. In 44 summary, our results suggest frequent evolutionary repeatability in shaping expression 45 difference associated with colonization of an alpine environment and support the hypothesis 46 of an important role of genetic variation in cis-regulatory elements in gene expression 47 parallelism.48 49

show abstract

“…The level of parallelism for gene expression abundance changes varies across study systems. In some taxa and natural conditions, significantly more genes show parallel changes (repeatedly up- or down-regulated in one ecotype relative to the other among independent population pairs) than anti-directional changes (Zhao et al 2015; Hart et al 2018; Kitano et al 2018; McGirr and Martin. 2018).…”

Section: Introductionmentioning

confidence: 99%

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Huang

Lack

Hoppel

et al. 2019

Preprint

View full text Add to dashboard Cite

17Changes in gene regulation at multiple levels may comprise an important share of the molecular 18 changes underlying adaptive evolution in nature. However, few studies have assayed within-and 19 between-population variation in gene regulatory traits at a transcriptomic scale, and therefore 20 inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess 21 quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) 22 between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting 23 thermal environments that reflect three separate instances of cold tolerance evolution. The cold-24 adapted populations were known to show population genetic evidence for parallel evolution at the 25 SNP level, and here we find significant although somewhat limited evidence for parallel expression 26 evolution between them, and less evidence for parallel splicing evolution. We find that genes with 27 mitochondrial functions are particularly enriched among candidates for adaptive expression 28 evolution. We also develop a method to estimate cis-versus trans-encoded contributions to 29 expression or splicing differences that does not rely on the presence of fixed differences between 30 parental strains. Applying this method, we infer important roles of both cis-and trans-regulation 31 among our putatively adaptive expression and splicing differences. The apparent contributions of cis-32 versus trans-regulation to adaptive evolution vary substantially among population pairs, with an 33 Ethiopian pair showing pervasive trans-effects, suggesting that basic characteristics of regulatory 34 evolution may depend on biological context. These findings expand our knowledge of adaptive gene 35 regulatory evolution and our ability to make inferences about this important and widespread process.36 37 50 The level of parallelism for gene expression abundance changes varies across study systems. In some 51 taxa and natural conditions, significantly more genes show parallel changes (repeatedly up-or down-52 regulated in one ecotype relative to the other among independent population pairs) than anti-53 directional changes (Zhao et al. 2015; Hart et al. 2018; Kitano et al. 2018; McGirr and Martin.54 2018). However, some other cases did not show significant parallel patterns, or they even show anti-55 parallel patterns (Derome et al. 2006; Lai et al. 2008; Hanson et al. 2017). The varying degree of 56 parallelism may partly be explained by the level of divergence among ancestors: more closely related 57 ancestors are expected to show a higher degree of parallel genetic evolution underlie similar 58 phenotypic evolution (Conte et al. 2012; Rosenblum et al. 2014). 59 60 Furthermore, gene expression evolution can be caused by the same or different molecular 61 underpinnings. Because of the difficulties of mapping expression QTL, a first step is to classify the 62 expression evolution into two regulatory classes. Cis-regulatory change...

show abstract

Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies

Cited by 32 publications

References 76 publications

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

Parallelism in gene expression between foothill and alpine ecotypes in Arabidopsis arenosa

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

Contact Info

Product

Resources

About