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

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

eLife ◽

10.7554/elife.67485 ◽

2021 ◽

Vol 10 ◽

Author(s):

Mathias Scharmann ◽

Anthony G Rebelo ◽

John R Pannell

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Positive Association ◽

Leaf Size ◽

Sex Bias ◽

Evolution Of Sex ◽

Rates Of Evolution ◽

Expression Evolution ◽

Species Specific ◽

And Shifts

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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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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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 in the Drosophila metabolome increases throughout development

10.1101/073148 ◽

2016 ◽

Author(s):

FC Ingleby ◽

Edward H Morrow

Keyword(s):

Gene Expression ◽

Sexual Dimorphism ◽

Metabolic Profiling ◽

Evolutionary Biology ◽

General Pattern ◽

Sexually Dimorphic ◽

Transcriptomic Data ◽

Expression Studies ◽

Males And Females ◽

Gene Expression Studies

AbstractThe expression of sexually dimorphic phenotypes from a shared genome between males and females is a longstanding puzzle in evolutionary biology. Increasingly, research has made use of transcriptomic technology to examine the molecular basis of sexual dimorphism through gene expression studies, but even this level of detail misses the metabolic processes that ultimately link gene expression with the whole organism phenotype. We use metabolic profiling in Drosophila melanogaster to complete this missing step, with a view to examining variation in male and female metabolic profiles, or metabolomes, throughout development. We show that the metabolome varies considerably throughout larval, pupal and adult stages. We also find significant sexual dimorphism in the metabolome, although only in pupae and adults, and the extent of dimorphism tends to increase throughout development. We compare this to transcriptomic data from the same population and find that the general pattern of increasing sex differences throughout development is mirrored in RNA expression. We discuss our results in terms of the usefulness of metabolic profiling in linking genotype and phenotype to more fully understand the basis of sexually dimorphic phenotypes.

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Intra- and inter-specific variations of gene expression levels in yeast are largely neutral

10.1101/089995 ◽

2016 ◽

Cited By ~ 1

Author(s):

Jian-Rong Yang ◽

Calum Maclean ◽

Chungoo Park ◽

Huabin Zhao ◽

Jianzhi Zhang

Keyword(s):

Gene Expression ◽

Genome Sequence ◽

Large Fraction ◽

General Role ◽

Expression Levels ◽

Genome Wide ◽

Sequence Variations ◽

Expression Evolution ◽

Molecular Phenotypes ◽

Gene Expression Levels

ABSTRACTIt is commonly, although not universally, accepted that most intra- and inter-specific genome sequence variations are more or less neutral, whereas a large fraction of organism-level phenotypic variations are adaptive. Gene expression levels are molecular phenotypes that bridge the gap between genotypes and corresponding organism-level phenotypes. Yet, it is unknown whether natural variations in gene expression levels are mostly neutral or adaptive. Here we address this fundamental question by genome-wide profiling and comparison of gene expression levels in nine yeast strains belonging to three closely related Saccharomyces species and originating from five different ecological environments. We find that the transcriptome-based clustering of the nine strains approximates the genome sequence-based phylogeny irrespective of their ecological environments. Remarkably, only ∼0.5% of genes exhibit similar expression levels among strains from a common ecological environment, no greater than that among strains with comparable phylogenetic relationships but different environments. These and other observations strongly suggest that most intra- and inter-specific variations in yeast gene expression levels result from the accumulation of random mutations rather than environmental adaptations. This finding has profound implications for understanding the driving force of gene expression evolution, genetic basis of phenotypic adaptation, and general role of stochasticity in evolution.

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Variable Rates of Simple Satellite Gains across the Drosophila Phylogeny

Molecular Biology and Evolution ◽

10.1093/molbev/msy005 ◽

2018 ◽

Vol 35 (4) ◽

pp. 925-941 ◽

Cited By ~ 31

Author(s):

Kevin H -C Wei ◽

Sarah E Lower ◽

Ian V Caldas ◽

Trevor J S Sless ◽

Daniel A Barbash ◽

...

Keyword(s):

Evolutionary Dynamics ◽

Rapid Evolution ◽

Single Mutation ◽

Closely Related Species ◽

Interspecific Differences ◽

Limited Sampling ◽

Drosophila Phylogeny ◽

Males And Females ◽

Species Specific ◽

Turn Over

Abstract Simple satellites are tandemly repeating short DNA motifs that can span megabases in eukaryotic genomes. Because they can cause genomic instability through nonallelic homologous exchange, they are primarily found in the repressive heterochromatin near centromeres and telomeres where recombination is minimal, and on the Y chromosome, where they accumulate as the chromosome degenerates. Interestingly, the types and abundances of simple satellites often vary dramatically between closely related species, suggesting that they turn over rapidly. However, limited sampling has prevented detailed understanding of their evolutionary dynamics. Here, we characterize simple satellites from whole-genome sequences generated from males and females of nine Drosophila species, spanning 40 Ma of evolution. We show that PCR-free library preparation and postsequencing GC-correction better capture satellite quantities than conventional methods. We find that over half of the 207 simple satellites identified are species-specific, consistent with previous descriptions of their rapid evolution. Based on a maximum parsimony framework, we determined that most interspecific differences are due to lineage-specific gains. Simple satellites gained within a species are typically a single mutation away from abundant existing satellites, suggesting that they likely emerge from existing satellites, especially in the genomes of satellite-rich species. Interestingly, unlike most of the other lineages which experience various degrees of gains, the lineage leading up to the satellite-poor D. pseudoobscura and D. persimilis appears to be recalcitrant to gains, providing a counterpoint to the notion that simple satellites are universally rapidly evolving.

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Cuticular hydrocarbons for identifying Sarcophagidae (Diptera)

Scientific Reports ◽

10.1038/s41598-021-87221-y ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Hannah E. Moore ◽

Martin J. R. Hall ◽

Falko P. Drijfhout ◽

Robert B. Cody ◽

Daniel Whitmore

Keyword(s):

Cuticular Hydrocarbons ◽

Gas Chromatography Mass Spectrometry ◽

Sexually Dimorphic ◽

Adult Males ◽

History Museum ◽

Chemical Profiles ◽

Males And Females ◽

Species Specific ◽

Flesh Flies ◽

Eleven Species

AbstractThe composition and quantity of insect cuticular hydrocarbons (CHCs) can be species-specific as well as sexually dimorphic within species. CHC analysis has been previously used for identification and ageing purposes for several insect orders including true flies (Diptera). Here, we analysed the CHC chemical profiles of adult males and females of eleven species of flesh flies belonging to the genus Sarcophaga Meigen (Sarcophagidae), namely Sarcophaga africa (Wiedemann), S. agnata Rondani, S. argyrostoma Robineau-Desvoidy, S. carnaria (Linnaeus), S. crassipalpis Macquart, S. melanura Meigen, S. pumila Meigen, S. teretirostris Pandellé, S. subvicina Rohdendorf, S. vagans Meigen and S. variegata (Scopoli). Cuticular hydrocarbons extracted from pinned specimens from the collections of the Natural History Museum, London using a customised extraction technique were analysed using Gas Chromatography–Mass Spectrometry. Time of preservation prior to extraction ranged between a few weeks to over one hundred years. CHC profiles (1) allowed reliable identification of a large majority of specimens, (2) differed between males and females of the same species, (3) reliably associated males and females of the same species, provided sufficient replicates (up to 10) of each sex were analysed, and (4) identified specimens preserved for up to over one hundred years prior to extraction.

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Sex differences in gene expression and proliferation are dependent on the epigenetic modifier HP1γ

10.1101/563940 ◽

2019 ◽

Author(s):

Pui-Pik Law ◽

Ping-Kei Chan ◽

Kirsten McEwen ◽

Huihan Zhi ◽

Bing Liang ◽

...

Keyword(s):

Gene Expression ◽

Sex Differences ◽

Sex Chromosome ◽

Chromosome Complement ◽

Autosomal Gene ◽

Sexually Dimorphic ◽

Heterochromatin Protein 1 ◽

Epigenetic Modifier ◽

Early Embryos ◽

Males And Females

SummarySex differences in growth rate in very early embryos have been recognized in a variety of mammals and attributed to sex-chromosome complement effects as they occur before overt sexual differentiation. We previously found that sex-chromosome complement, rather than sex hormones regulates heterochromatin-mediated silencing of a transgene and autosomal gene expression in mice. Here, sex dimorphism in proliferation was investigated. We confirm that male embryonic fibroblasts proliferate faster than female fibroblasts and show that this proliferation advantage is completely dependent upon heterochromatin protein 1 gamma (HP1γ). To determine whether this sex-regulatory effect of HP1γ was a more general phenomenon, we performed RNA sequencing on MEFs derived from males and females, with or without HP1γ. Strikingly, HP1γ was found to be crucial for regulating nearly all sexually dimorphic autosomal gene expression because deletion of the HP1γ gene in males abolished sex differences in autosomal gene expression. The identification of a key epigenetic modifier as central in defining gene expression differences between males and females has important implications for understanding physiological sex differences and sex bias in disease.

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Heterospecific aggression differs predominately by species, rather than sex, in Lake Malawi cichlid fish

10.1101/720375 ◽

2019 ◽

Cited By ~ 1

Author(s):

Emily C. Moore ◽

Reade B. Roberts

Keyword(s):

Community Structure ◽

Rapid Evolution ◽

Cichlid Fish ◽

Lake Malawi ◽

Male Aggression ◽

Males And Females ◽

Potential Impact ◽

Cortisol Levels ◽

Species Specific ◽

Heterospecific Aggression

ABSTRACTBecause of their striking diversity, Lake Malawi cichlid fish have been well studied for male aggression, particularly among dominant males of closely related sister species within the framework of mate-choice and speciation. However, aggression in females has been largely ignored, and variation in aggressive behaviors between more distantly-related taxa is not well understood despite its potential impact in a complex community structure. To better understand variation in patterns of aggression between species, we presented males and females from five species of Lake Malawi cichlid with a non-predator intruder and recorded all movement and aggressive acts. Additionally, we measured excreted cortisol levels the day after the intruder assay to evaluate one physiological aspect of stress response. We identified species-specific patterns in both specific aggressive acts, and overall level of aggression. Additionally, we found that sexual dimorphism in aggressive acts varies by species and act, where the species with the most aggressive males also has aggressive females. Additionally, cortisol levels vary by taxa, and are associated with restless behavior in the intruder assay, but not levels of aggression. These findings have bearing on understanding sex differences in aggression and their impact on community structure in this important model of rapid evolution.

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Sex bias evaluation of classic and novel Housekeeping Genes in adipose tissue through the massive analysis of transcriptomics data

10.1101/2021.12.04.471124 ◽

2021 ◽

Author(s):

Maria Guaita-Cespedes ◽

Rubén Grillo-Risco ◽

Marta R. Hidalgo ◽

Sonia Fernández-Veledo ◽

Deborah Burks ◽

...

Keyword(s):

Gene Expression ◽

Adipose Tissue ◽

Expression Profiles ◽

Housekeeping Genes ◽

Sex Bias ◽

Expression Stability ◽

Expression Levels ◽

Cell Functions ◽

Web Resource ◽

New Genes

ABSTRACTHousekeeping genes (HKG), those involved in the maintenance of basic cell functions, are considered to have constant expression levels in all cell types, and are therefore commonly used as internal controls in gene expression studies. Nevertheless, multiple studies have shown that not all of them have stable expression levels across different cells, tissues, and conditions, introducing a systematic error in the experimental results. The proper selection and validation of control housekeeping genes in the specific studied conditions is crucial for the validity of the obtained results, although, up to date, sex has never been taken into account as a biological variable.In this work, we evaluate the expression profiles of six classical housekeeping genes, (four metabolic: HPRT, GAPDH, PPIA and UBC, and two ribosomal: 18S and RPL19) used as controls in several tissues, to determine the stability of their expression in adipose tissue of Homo sapiens and Mus musculus and asses sex bias and control suitability. We also evaluated gene expression stability of the genes included in different whole transcriptome microarrays available at the Gene Expression Omnibus database (GEO), to identify new genes suitable to be used as sex-unbiased controls. We perform a sex-based analysis to test for/reveal sexual dimorphism of mRNA expression stability.We use a novel computational strategy based on meta-analysis techniques which evidence that some classical housekeeping genes do not fit to analyze human adipose tissue when sex variable is included. For instance, the extensively used 18S has shown to be variable in this tissue, while PPIA and RPL19 have shown to be good HKG targets. Further, we propose new sex-unbiased human and mouse housekeeping genes, derived from sex-specific expression profiles, including, RPS8 or UBB. All the results generated in this work are available in an open web resource (https://bioinfo.cipf.es/metafun-HKG), so that they can be consulted and used in further studies.

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