Rapid Evolution of Ovarian-Biased Genes in the Yellow Fever Mosquito (<i>Aedes aegypti</i>)

Whittle, Carrie A.; Extavour, Cassandra G.

doi:10.1534/genetics.117.201343

Cited by 24 publications

(78 citation statements)

References 127 publications

(233 reference statements)

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“…Perhaps selection in mtDNA that contributes to sexspecific traits (sexually dimorphic or sexually antagonistic) may be a mechanism for the Ae. aegypti ovaries to evolve rapidly (Innocenti et al 2011;Whittle and Extavour 2017). Genes in the reproductive tissues contributing to the sexual and reproductive functions are often rapidly evolving (Jagadeeshan and Singh 2005).…”

Section: Discussionmentioning

confidence: 99%

“…Genes expressed in the germline of males and females are believed to play an important role in evolution, contributing to reproductive fitness, isolation, and speciation (Whittle and Extavour 2017). Thus it is an important step to study the role of sex-biased gonad genes in evolution.…”

Section: Sex Specific Gene Expression Overviewmentioning

confidence: 99%

“…aegypti exhibits fast evolution of ovary-biased genes compared to Drosophila melanogaster and Ae. albopictus (Whittle and Extavour 2017).…”

Section: Female Germline (Nbf and Pbm 36hr Ovaries)mentioning

confidence: 99%

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The Developmental Transcriptome ofAe. albopictus,a Major Worldwide Human Disease Vector

Gamez¹,

Antoshechkin

Méndez‐Sánchez

et al. 2019

Preprint

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Aedes albopictus mosquitoes are important vectors for a number of human pathogens including the Zika, dengue, and chikungunya viruses. Capable of displacing Aedes aegypti populations, it adapts to cooler environments which increases its geographical range and transmission potential. There are limited control strategies for Aedes albopictus mosquitoes which is likely attributed to the lack of comprehensive biological studies on this emerging vector. To fill this void, here using RNAseq we characterized Aedes albopictus mRNA expression profiles at 47 distinct time points throughout development providing the first high-resolution comprehensive view of the developmental transcriptome of this worldwide human disease vector. This enabled us to identify several patterns of shared gene expression among tissues as well as sex-specific expression patterns. Moreover, to illuminate the similarities and differences between Aedes aegypti, a related human disease vector, we performed a comparative analysis using the two developmental transcriptomes. We identify life stages were the two species exhibited significant differential expression among orthologs. These findings provide insights into the similarities and differences between Aedes albopictus and Aedes aegypti mosquito biology. In summary, the results generated from this study should form the basis for future investigations on the biology of Aedes albopictus mosquitoes and provide a goldmine resource for the development of transgene-based vector control strategies.

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Section: Discussionmentioning

confidence: 99%

Section: Sex Specific Gene Expression Overviewmentioning

confidence: 99%

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The Developmental Transcriptome ofAe. albopictus,a Major Worldwide Human Disease Vector

Gamez¹,

Antoshechkin

Méndez‐Sánchez

et al. 2019

Preprint

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“…Expression was compared between the testes and ovaries, and between GT-males and GT-females by using Deseq2 to obtain P-values [44] and the average FPKM of the replicates per tissue type (Table S1). Any gene having at least a two-fold difference in average expression and a statistically significant P-value (P<0.05) as well as a FPKM of at least one in one tissue type was identified as sex-biased [17, 73]. All other genes with nonzero expression in gonadal and in nongonadal contrasts were defined as unbiased.…”

Section: Methodsmentioning

confidence: 99%

Absence of a faster-X effect in beetles (Tribolium, Coleoptera)

Whittle

Kulkarni

Extavour

2019

Preprint

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1Background. The faster-X effect, namely the rapid evolution of protein-coding genes on the X-chromosome, 2 has been reported in numerous metazoans. However, the prevalence of this phenomenon across metazoans and 3 its potential causes remain largely unresolved. Analysis of sex-biased genes may elucidate its possible 4 mechanisms: a more pronounced faster-X effect in male-biased genes than in female-biased or unbiased genes, 5 suggests fixation of recessive beneficial mutations rather than genetic drift. Further, theory predicts that the 6 faster-X effect should be promoted by X-chromosome dosage compensation, but this topic remains rarely 7 empirically examined. 8 9Results. Here, we asked whether we could detect a faster-X effect in genes of the beetle Tribolium castaneum 10 (and T. freemani orthologs), which has X/Y sex-determination and heterogametic males. Our comparison of 11 protein sequence divergence (dN/dS) on the X-chromosome versus autosomes indicated the complete absence 12 of a faster-X effect. Further, analyses of sex-biased gene expression revealed that the X-chromosome was 13 strongly enriched for ovary-biased genes, which evolved under exceptionally high constraint. An evaluation of 14 male X-chromosome dosage compensation in the gonads and in non-gonadal somatic tissues showed an 15 extreme lack of compensation in the testis. This under-expression of the X chromosome in males may limit the 16 phenotypic effect, and therefore likelihood of fixation, of recessive beneficial X-linked mutations in genes 17 transcribed in male gonads. 19Conclusions. We show that these beetles display a rare unequivocal example of the absence of a faster-X effect 20 in a metazoan. We propose two potential causes for this, namely high constraint on X-linked ovary-biased 21 genes, and an extreme lack of dosage compensation of genes transcribed in the testis. 23Keywords: Tribolium castaneum, faster-X, sex-biased expression, dosage compensation, dN/dS 24 25 53 chromosome and autosomes, revealed a faster-X effect for all three classes of sex biased genes 54 (male-biased, female-based and unbiased). In this study, protein sequence divergence was 55 highest in male-biased genes and lowest in female-biased genes, empirically supporting a model 56 4 of fixation of beneficial mutations on the X chromosome [15, 16]. In chickens, which have WZ 57 sex chromosomes and female heterogamy, elevated dN/dS has been reported across all studied 58 genes on the Z-chromosome, consistent with the faster-X (or faster-Z in this case) effect [21]. 59 However, the prediction of higher dN/dS for female-biased genes on the Z-chromosome was not 60 met in this study, suggesting that the faster-Z in these birds was not due to fixation of recessive 61 beneficial mutations, and rather might be attributable to fixation of neutral or slightly deleterious 62 mutations via genetic drift [7, 16]. Recently, similar results were reported for the W/Z 63 chromosomes of Heliconius butterflies [14]. At present however, the study of the faster-X effect, 64 i...

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“…Expression was compared between the testes and ovaries, and between GT-males and GT-females by using Deseq2 to obtain P-values (Love et al 2014) and the average FPKM of the replicates per tissue type (Table S1). Any gene having at least a twofold difference in average expression (Mank et al 2010a;Assis et al 2012;Whittle and Extavour 2017) and having a statistically significant P-value in Deseq2 (P , 0.05) as well as a FPKM of at least one in one tissue type was identified as sex-biased. All other genes were defined as unbiased.…”

Section: Gene Expression and Identification Of Sex-biased Genesmentioning

confidence: 99%

Absence of a Faster-X Effect in Beetles (Tribolium, Coleoptera)

Whittle

Kulkarni

Extavour

2020

G3 Genes|Genomes|Genetics

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The faster-X effect, namely the rapid evolution of protein-coding genes on the X chromosome, has been widely reported in metazoans. However, the prevalence of this phenomenon across diverse systems and its potential causes remain largely unresolved. Analysis of sex-biased genes may elucidate its possible mechanisms: for example, in systems with X/Y males a more pronounced faster-X effect in male-biased genes than in female-biased or unbiased genes may suggest fixation of recessive beneficial mutations rather than genetic drift. Further, theory predicts that the faster-X effect should be promoted by X chromosome dosage compensation. Here, we asked whether we could detect a faster-X effect in genes of the beetle Tribolium castaneum (and T. freemani orthologs), which has X/Y sex-determination and heterogametic males. Our comparison of protein sequence divergence (dN/dS) on the X chromosome vs. autosomes indicated a rarely observed absence of a faster-X effect in this organism. Further, analyses of sex-biased gene expression revealed that the X chromosome was particularly highly enriched for ovary-biased genes, which evolved slowly. In addition, an evaluation of male X chromosome dosage compensation in the gonads and in non-gonadal somatic tissues indicated a striking lack of compensation in the testis. This under-expression in testis may limit fixation of recessive beneficial X-linked mutations in genes transcribed in these male sex organs. Taken together, these beetles provide an example of the absence of a faster-X effect on protein evolution in a metazoan, that may result from two plausible factors, strong constraint on abundant X-linked ovary-biased genes and a lack of gonadal dosage compensation.

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Rapid Evolution of Ovarian-Biased Genes in the Yellow Fever Mosquito (Aedes aegypti)

Cited by 24 publications

References 127 publications

The Developmental Transcriptome ofAe. albopictus,a Major Worldwide Human Disease Vector

The Developmental Transcriptome ofAe. albopictus,a Major Worldwide Human Disease Vector

Absence of a faster-X effect in beetles (Tribolium, Coleoptera)

Absence of a Faster-X Effect in Beetles (Tribolium, Coleoptera)

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