Rapid evolution of female-biased genes among four species of <i>Anopheles</i> malaria mosquitoes

Comparative genomics has become a central tool for evolutionary biology, and a better knowledge of understudied taxa represents the foundation for future work. In this study, we characterized the transcriptome of male and female mature gonads in the European clam Ruditapes decussatus, compared with that in the Manila clam Ruditapes philippinarum providing, for the first time in bivalves, information about transcription dynamics and sequence evolution of sex-biased genes. In both the species, we found a relatively low number of sex-biased genes (1,284, corresponding to 41.3% of the orthologous genes between the two species), probably due to the absence of sexual dimorphism, and the transcriptional bias is maintained in only 33% of the orthologs. The dN/dS is generally low, indicating purifying selection, with genes where the female-biased transcription is maintained between the two species showing a significantly higher dN/dS. Genes involved in embryo development, cell proliferation, and maintenance of genome stability show a faster sequence evolution. Finally, we report a lack of clear correlation between transcription level and evolutionary rate in these species, in contrast with studies that reported a negative correlation. We discuss such discrepancy and call into question some methodological approaches and rationales generally used in this type of comparative studies.

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“…2007 ), and similar patterns were found in copepods ( Poley et al. 2016 ), Anopheles ( Papa et al. 2017 ), fish ( Small et al.…”

Section: Discussionsupporting

confidence: 63%

Comparative Transcriptomics in Two Bivalve Species Offers Different Perspectives on the Evolution of Sex-Biased Genes

Ghiselli

Iannello

Puccio

et al. 2018

Genome Biology and Evolution

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“…In addition, female-biased genes also evolve significantly faster than unbiased genes in Anastrepha species, which has also been described for some animal taxa such as birds ( Mank et al. 2007 ), mosquitoes ( Papa et al. 2017 ; Whittle and Extavour 2017 ), and fishes ( Yang et al.…”

Section: Discussionsupporting

confidence: 52%

Evidence of Adaptive Evolution and Relaxed Constraints in Sex-Biased Genes of South American and West Indies Fruit Flies (Diptera: Tephritidae)

Congrains¹,

Campanini²,

Torres³

et al. 2018

Genome Biology and Evolution

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Several studies have demonstrated that genes differentially expressed between sexes (sex-biased genes) tend to evolve faster than unbiased genes, particularly in males. The reason for this accelerated evolution is not clear, but several explanations have involved adaptive and nonadaptive mechanisms. Furthermore, the differences of sex-biased expression patterns of closely related species are also little explored out of Drosophila. To address the evolutionary processes involved with sex-biased expression in species with incipient differentiation, we analyzed male and female transcriptomes of Anastrepha fraterculus and Anastrepha obliqua, a pair of species that have diverged recently, likely in the presence of gene flow. Using these data, we inferred differentiation indexes and evolutionary rates and tested for signals of selection in thousands of genes expressed in head and reproductive transcriptomes from both species. Our results indicate that sex-biased and reproductive-biased genes evolve faster than unbiased genes in both species, which is due to both adaptive pressure and relaxed constraints. Furthermore, among male-biased genes evolving under positive selection, we identified some related to sexual functions such as courtship behavior and fertility. These findings suggest that sex-biased genes may have played important roles in the establishment of reproductive isolation between these species, due to a combination of selection and drift, and unveil a plethora of genetic markers useful for more studies in these species and their differentiation.

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“…Intriguingly, this unusual ovary-biased signature in young genes is reminiscent of recent findings from another human disease vector, mosquito (Anopheles spp. ; Papa et al. 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera

Helleu

Levine

2018

Molecular Biology and Evolution

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The heterochromatic genome compartment mediates strictly conserved cellular processes such as chromosome segregation, telomere integrity, and genome stability. Paradoxically, heterochromatic DNA sequence is wildly unconserved. Recent reports that many hybrid incompatibility genes encode heterochromatin proteins, together with the observation that interspecies hybrids suffer aberrant heterochromatin-dependent processes, suggest that heterochromatic DNA packaging requires species-specific innovations. Testing this model of coevolution between fast-evolving heterochromatic DNA and its packaging proteins begins with defining the latter. Here we describe many such candidates encoded by the Heterochromatin Protein 1 (HP1) gene family across Diptera, an insect Order that encompasses dramatic episodes of heterochromatic sequence turnover. Using BLAST, synteny analysis, and phylogenetic tree building across 64 Diptera genomes, we discovered a staggering 121 HP1 duplication events. In contrast, we observed virtually no gene duplication in gene families that share a common “chromodomain” with HP1s, including Polycomb and Su(var)3-9. The remarkably high number of Dipteran HP1 paralogs arises from distant clades undergoing convergent HP1 family amplifications. These independently derived, young HP1s span diverse ages, domain structures, and rates of molecular evolution, including episodes of positive selection. Moreover, independently derived HP1s exhibit convergent expression evolution. While ancient HP1 parent genes are transcribed ubiquitously, young HP1 paralogs are transcribed primarily in male germline tissue, a pattern typical of young genes. Pervasive gene youth, rapid evolution, and germline specialization implicate heterochromatin-encoded selfish elements driving recurrent HP1 gene family expansions. The 121 young genes offer valuable experimental traction for elucidating the germline processes shaped by Diptera’s many dramatic episodes of heterochromatin turnover.

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Rapid evolution of female-biased genes among four species of Anopheles malaria mosquitoes

Cited by 65 publications

References 65 publications

Comparative Transcriptomics in Two Bivalve Species Offers Different Perspectives on the Evolution of Sex-Biased Genes

Comparative Transcriptomics in Two Bivalve Species Offers Different Perspectives on the Evolution of Sex-Biased Genes

Evidence of Adaptive Evolution and Relaxed Constraints in Sex-Biased Genes of South American and West Indies Fruit Flies (Diptera: Tephritidae)

Recurrent Amplification of the Heterochromatin Protein 1 (HP1) Gene Family across Diptera

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