High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

Differences between males and females are usually more subtle in dioecious plants than animals, but strong sexual dimorphism has evolved convergently in the South African Cape plant genus Leucadendron. Such sexual dimorphism in leaf size is expected largely to be due to differential gene expression between the sexes. We compared patterns of gene expression in leaves among ten Leucadendron species across the genus. Surprisingly, we found no positive association between sexual dimorphism in morphology and the number or the percentage of sex-biased genes. Sex bias in most sex-biased genes evolved recently and was species-specific. We compared rates of evolutionary change in expression for genes that were sex-biased in one species but unbiased in others and found that sex-biased genes evolved faster in expression than un-biased genes. This greater rate of expression evolution of sex-biased genes, also documented in animals, might suggest the possible role of sexual selection in the evolution of gene expression. However, our comparative analysis clearly indicates that the more rapid rate of expression evolution of sex-biased genes predated the origin of bias, and shifts towards bias were depleted in signatures of adaptation. Our results are thus more consistent with the view that sex bias is simply freer to evolve in genes less subject to constraints in expression level.

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High rates of evolution preceded shifts to sex-biased gene expression in Leucadendron, the most sexually dimorphic angiosperms

10.1101/2021.01.12.426328 ◽

2021 ◽

Author(s):

Mathias Scharmann ◽

Anthony G Rebelo ◽

John R Pannell

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Rapid Evolution ◽

Sex Bias ◽

Sexually Dimorphic ◽

Expression Levels ◽

Rates Of Evolution ◽

Expression Evolution ◽

Males And Females ◽

Species Specific

AbstractThe males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munné-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.

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The evolution of sex-biased gene expression in the Drosophila brain

10.1101/2020.04.14.041624 ◽

2020 ◽

Cited By ~ 1

Author(s):

Samuel Khodursky ◽

Nicolas Svetec ◽

Sylvia Durkin ◽

Li Zhao

Keyword(s):

Gene Expression ◽

X Chromosome ◽

Sexually Dimorphic ◽

Evolution Of Sex ◽

Sequencing Data ◽

Regulatory Changes ◽

Drosophila Brain ◽

Expression Evolution ◽

Species Specific ◽

Flanking Regions

AbstractGenes with sex-biased expression in Drosophila are thought to underlie sexually dimorphic phenotypes and have been shown to possess important evolutionary properties. However, the forces and constraints governing the evolution of sex-biased genes in the somatic tissues of Drosophila are largely unknown. Using population-scale RNA sequencing data we show that sex-biased genes in the Drosophila brain are highly enriched on the X Chromosome and that most are biased in a species-specific manner. We show that X-linked male-biased genes, and to a lesser extent female-biased genes, are enriched for signatures of directional selection at the gene expression level. By examining the evolutionary properties of gene flanking regions on the X Chromosome, we find evidence that adaptive cis-regulatory changes are more likely to drive the expression evolution of X-linked male-biased genes than other X-linked genes. Finally, we examine whether constraint due to broad expression across multiple tissues and genetic constraint due to the largely shared male and female genomes could be responsible for the observed patterns of gene expression evolution. We find that expression breadth does not constrain the directional evolution of gene expression in the brain. Additionally, we find that the shared genome between males and females imposes a substantial constraint on the expression evolution of sex-biased genes. Overall, these results significantly advance our understanding of the patterns and forces shaping the evolution of sexual dimorphism in the Drosophila brain.

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Sexual Dimorphism and the Evolution of Sex-Biased Gene Expression in the Brown Alga Ectocarpus

Molecular Biology and Evolution ◽

10.1093/molbev/msv049 ◽

2015 ◽

Vol 32 (6) ◽

pp. 1581-1597 ◽

Cited By ~ 55

Author(s):

Agnieszka Lipinska ◽

Alexandre Cormier ◽

Rémy Luthringer ◽

Akira F. Peters ◽

Erwan Corre ◽

...

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Brown Alga ◽

Evolution Of Sex

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Sex-biased expression between guppies varying in the presence of ornamental coloration

PeerJ ◽

10.7717/peerj.5782 ◽

2018 ◽

Vol 6 ◽

pp. e5782 ◽

Cited By ~ 2

Author(s):

Cynthia Dick ◽

David N. Reznick ◽

Cheryl Y. Hayashi

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Differential Expression ◽

Differentially Expressed ◽

Sex Bias ◽

Melanin Synthesis ◽

A Genome ◽

Visual Color ◽

Color Differences ◽

Whole Transcriptome

Sex-biased gene expression provides a means to achieve sexual dimorphism across a genome largely shared by both sexes. Trinidadian guppies are ideal to examine questions of sex-bias as they exhibit sexual dimorphism in ornamental coloration with male only expression. Here we use RNA-sequencing to quantify whole transcriptome gene expression differences, with a focus on differential expression of color genes between the sexes. We determine whether males express genes positively correlated with coloration at higher levels than females. We find that all the differentially expressed color genes were more highly expressed by males. Males also expressed all known black melanin synthesis genes at higher levels than females, regardless of whether the gene was significantly differentially expressed in the analysis. These differences correlated with the visual color differences between sexes at the stage sampled, as all males had ornamental black coloration apparent. We propose that sexual dimorphism in ornamental coloration is caused by male-biased expression of color genes.

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How different is the evolution of sex-biased gene expression between plants and animals? A commentary on: ‘Sexual dimorphism and rapid turnover in gene expression in pre-reproductive seedlings of a dioecious herb’

Annals of Botany ◽

10.1093/aob/mcz081 ◽

2019 ◽

Vol 123 (7) ◽

pp. iv-v ◽

Cited By ~ 3

Author(s):

Aline Muyle

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Evolution Of Sex ◽

Rapid Turnover

This article comments on: Guillaume G. Cossard, Melissa A. Toups and John R. Pannell. 2019. Sexual dimorphism and rapid turnover in gene expression in pre-reproductive seedlings of a dioecious herb. Annals of Botany 123(7): 1119–1131.

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Sexual Dimorphism in Growth Rate and Gene Expression Throughout Immature Development in Wild Type Chrysomya rufifacies (Diptera: Calliphoridae) Macquart

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.696638 ◽

2021 ◽

Vol 9 ◽

Author(s):

Meaghan L. Pimsler ◽

Carl E. Hjelmen ◽

Michelle M. Jonika ◽

Anika Sharma ◽

Shuhua Fu ◽

...

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Sex Determination ◽

Splice Variants ◽

Expression Patterns ◽

Relevant Information ◽

Wild Type ◽

Chrysomya Rufifacies ◽

Immature Development ◽

Species Specific

Reliability of forensic entomology analyses to produce relevant information to a given case requires an understanding of the underlying arthropod population(s) of interest and the factors contributing to variability. Common traits for analyses are affected by a variety of genetic and environmental factors. One trait of interest in forensic investigations has been species-specific temperature-dependent growth rates. Recent work indicates sexual dimorphism may be important in the analysis of such traits and related genetic markers of age. However, studying sexual dimorphic patterns of gene expression throughout immature development in wild-type insects can be difficult due to a lack of genetic tools, and the limits of most sex-determination mechanisms. Chrysomya rufifacies, however, is a particularly tractable system to address these issues as it has a monogenic sex determination system, meaning females have only a single-sex of offspring throughout their life. Using modified breeding procedures (to ensure single-female egg clutches) and transcriptomics, we investigated sexual dimorphism in development rate and gene expression. Females develop slower than males (9 h difference from egg to eclosion respectively) even at 30°C, with an average egg-to-eclosion time of 225 h for males and 234 h for females. Given that many key genes rely on sex-specific splicing for the development and maintenance of sexually dimorphic traits, we used a transcriptomic approach to identify different expression of gene splice variants. We find that 98.4% of assembled nodes exhibited sex-specific, stage-specific, to sex-by-stage specific patterns of expression. However, the greatest signal in the expression data is differentiation by developmental stage, indicating that sexual dimorphism in gene expression during development may not be investigatively important and that markers of age may be relatively independent of sex. Subtle differences in these gene expression patterns can be detected as early as 4 h post-oviposition, and 12 of these nodes demonstrate homology with key Drosophila sex determination genes, providing clues regarding the distinct sex determination mechanism of C. rufifacies. Finally, we validated the transcriptome analyses through qPCR and have identified five genes that are developmentally informative within and between sexes.

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Character trees from transcriptome data: origin and individuation of morphological characters and the so-called “species signal”

10.1101/019380 ◽

2015 ◽

Cited By ~ 1

Author(s):

Jacob Musser ◽

Gunter Wagner

Keyword(s):

Gene Expression ◽

Concerted Evolution ◽

Morphological Character ◽

Morphological Characters ◽

Character Type ◽

Rigorous Testing ◽

History Of ◽

Expression Evolution ◽

Species Specific ◽

Development And Evolution

We elaborate a framework for investigating the evolutionary history of morphological characters. We argue that morphological character trees generated by phylogenetic analysis of transcriptomes provide a useful tool for identifying causal gene expression differences underlying the development and evolution of morphological characters. They also enable rigorous testing of different models of morphological character evolution and origination, including the hypothesis that characters originate via divergence of repeated ancestral characters. Finally, morphological character trees provide evidence that character transcriptomes undergo concerted evolution. We argue that concerted evolution of transcriptomes can explain the so-called ?species-specific clustering? found in several recent comparative transcriptome studies. The species signal is the phenomenon that transcriptomes cluster by species rather than character type, even though the characters are older than the respective species. We suggest that concerted gene expression evolution results from mutations that alter gene regulatory network interactions shared by the characters under comparison. Thus, character trees generated from transcriptomes allow us to investigate the variational independence, or individuation, of morphological characters at the level of genetic programs.

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Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Genetics ◽

10.1534/genetics.109.105775 ◽

2009 ◽

Vol 183 (3) ◽

pp. 1175-1185 ◽

Cited By ~ 39

Author(s):

Zi-Feng Jiang ◽

Carlos A. Machado

Keyword(s):

Gene Expression ◽

Natural Selection ◽

Sexual Dimorphism ◽

Sex Bias ◽

Drosophila Pseudoobscura ◽

Expression Divergence ◽

Behavioral Traits ◽

Mature Adults ◽

High Level ◽

Sexually Mature

Sexual dimorphism in morphological, physiological, and behavioral traits is pervasive in animals, as is the observation of strong sexual dimorphism in genomewide patterns of gene expression in the few species where this has been studied. Studies of transcriptome divergence show that most interspecific transcriptional divergence is highly sex dependent, an observation consistent with the action of sex-dependent natural selection during species divergence. However, few transcriptome evolution studies have been conducted between recently diverged species (<1 MY). Here, we present analyses of sex-biased transcriptome divergence in sexually mature adults of three recently diverged species of Drosophila: Drosophila pseudoobscura, D. persimilis, and D. pseudoobscura bogotana. Data were collected using a custom designed Agilent oligonucleotide. Expression was detected in 12,507 genes. About 80% of the expressed genes show sex-biased expression in each species. Across species, 21% of the transcriptome shows switches between nonsex bias and sex bias, and just 0.9% of the transcriptome shows reversals of sex-biased expression. Over 80% of the expression divergence between species is due to changes in one sex only. About 15% of the expression divergence between species is due to changes in the same direction in both sexes and just 2% is due to changes in both sexes but in opposite directions. In agreement with previous studies, we observe a high level of sex-dependent transcriptome divergence and strong demasculinization of the two arms of the X chromosome in all species. However, in contrast to previous studies we find that male-biased genes do not have higher levels of expression divergence than non-sex-biased genes, and sex-biased genes show higher levels of expression divergence in the alternate sex, suggesting that sex-biased genes endure stronger selection when expressed in the alternate sex.

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Drift and directional selection are the evolutionary forces driving gene expression divergence in eye and brain tissue ofHeliconiusbutterflies

10.1101/463174 ◽

2018 ◽

Author(s):

Ana Catalán ◽

Adriana Briscoe ◽

Sebastian Höhna

Keyword(s):

Gene Expression ◽

Brownian Motion ◽

Brain Tissue ◽

Directional Selection ◽

Stabilizing Selection ◽

Expression Levels ◽

Evolutionary Forces ◽

Expression Evolution ◽

Species Specific ◽

Gene Expression Evolution

AbstractInvestigating gene expression evolution over micro- and macroevolutionary timescales will expand our understanding of the role of gene expression in adaptation and speciation. In this study, we characterized which evolutionary forces are acting on gene expression levels in eye and brain tissue of fiveHeliconiusbutterflies with divergence times of ~5-12 MYA. We developed and applied Brownian motion and Ornstein-Uhlenbeck models to identify genes whose expression levels are evolving through drift, stabilizing selection, or a lineage-specific shift. We find that 81% of the genes evolve under genetic drift. When testing for branch-specific shifts in gene expression, we detected 368 (16%) shift events. Genes showing a shift towards up-regulation have significantly lower gene expression variance than those genes showing a shift leading towards down-regulation. We hypothesize that directional selection is acting in shifts causing up-regulation, since transcription is costly. We further uncover through simulations that parameter estimation of Ornstein-Uhlenbeck models is biased when using small phylogenies and only becomes reliable with phylogenies having at least 50 taxa. Therefore, we developed a new statistical test based on Brownian motion to identify highly conserved genes (i.e., evolving under strong stabilizing selection), which comprised 3% of the orthoclusters. In conclusion, we found that drift is the dominant evolutionary force driving gene expression evolution in eye and brain tissue inHeliconius. Nevertheless, the higher proportion of genes evolving under directional than under stabilizing selection might reflect species-specific selective pressures on vision and brain necessary to fulfill species-specific requirements.

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Gene expression evolution in pattern-triggered immunity within Arabidopsis thaliana and across Brassicaceae species

The Plant Cell ◽

10.1093/plcell/koab073 ◽

2021 ◽

Cited By ~ 1

Author(s):

Thomas M Winkelmüller ◽

Frederickson Entila ◽

Shajahan Anver ◽

Anna Piasecka ◽

Baoxing Song ◽

...

Keyword(s):

Gene Expression ◽

Arabidopsis Thaliana ◽

Binding Sites ◽

Expression Patterns ◽

Microbial Control ◽

Wrky Transcription Factor ◽

Specific Expression ◽

Brassicaceae Species ◽

Expression Evolution ◽

Species Specific

Abstract Plants recognize surrounding microbes by sensing microbe-associated molecular patterns (MAMPs) to activate pattern-triggered immunity (PTI). Despite their significance for microbial control, the evolution of PTI responses remains largely uncharacterized. Here, by employing comparative transcriptomics of six Arabidopsis thaliana accessions and three additional Brassicaceae species to investigate PTI responses, we identified a set of genes that commonly respond to the MAMP flg22 and genes that exhibit species-specific expression signatures. Variation in flg22-triggered transcriptome responses across Brassicaceae species was incongruent with their phylogeny, while expression changes were strongly conserved within A. thaliana. We found the enrichment of WRKY transcription factor binding sites in the 5′-regulatory regions of conserved and species-specific responsive genes, linking the emergence of WRKY-binding sites with the evolution of gene expression patterns during PTI. Our findings advance our understanding of the evolution of the transcriptome during biotic stress.

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