Hawaiian Drosophila as an Evolutionary Model Clade: Days of Future Past

O’Grady, Patrick M.; DeSalle, Rob

doi:10.1002/bies.201700246

Cited by 18 publications

(20 citation statements)

References 101 publications

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“…Such data could reveal sex-related networks relevant to both gonadal and nongonadal tissues, which may be valuable to understanding evolution of gonadal sex-biased expression. Further studies in this genus outside the melanogaster group, such as in the model Hawai’ian clade [80], may provide a particularly effective route for future assessments of the factors shaping evolution sex-biased gonadal expression.…”

Section: Discussionmentioning

confidence: 99%

Selection shapes turnover and magnitude of sex-biased expression in Drosophila gonads

Whittle

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2019

BMC Evol Biol

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Background Sex-biased gene expression is thought to drive the phenotypic differences in males and females in metazoans. Drosophila has served as a primary model for studying male-female differences in gene expression, and its effects on protein sequence divergence. However, the forces shaping evolution of sex-biased expression remain largely unresolved, including the roles of selection and pleiotropy. Research on sex organs in Drosophila, employing original approaches and multiple-species contrasts, provides a means to gain insights into factors shaping the turnover and magnitude (fold-bias) of sex-biased expression. Results Here, using recent RNA-seq data, we studied sex-biased gonadal expression in 10,740 protein coding sequences in four species of Drosophila, D. melanogaster , D. simulans , D. yakuba and D. ananassae (5 to 44 My divergence). Using an approach wherein we identified genes with lineage-specific transitions (LSTs) in sex-biased status (amongst testis-biased, ovary-biased and unbiased; thus, six transition types) standardized to the number of genes with the ancestral state (S-LSTs), and those with clade-wide expression bias status, we reveal several key findings. First, the six categorical types of S-LSTs in sex-bias showed disparate rates of turnover, consistent with differential selection pressures. Second, the turnover in sex-biased status was largely unrelated to cross-tissue expression breadth, suggesting pleiotropy does not restrict evolution of sex-biased expression. Third, the fold-sex-biased expression, for both testis-biased and ovary-biased genes, evolved directionally over time toward higher values, a crucial finding that could be interpreted as a selective advantage of greater sex-bias, and sexual antagonism. Fourth, in terms of protein divergence, genes with LSTs to testis-biased expression exhibited weak signals of elevated rates of evolution (than ovary-biased) in as little as 5 My, which strengthened over time. Moreover, genes with clade-wide testis-specific expression (44 My), a status not observed for any ovary-biased genes, exhibited striking acceleration of protein divergence, which was linked to low pleiotropy. Conclusions By studying LSTs and clade-wide sex-biased gonadal expression in a multi-species clade of Drosophila, we describe evidence that interspecies turnover and magnitude of sex-biased expression have been influenced by selection. Further, whilst pleiotropy was not connected to turnover in sex-biased gonadal expression, it likely explains protein sequence divergence. Electronic supplementary material The online version of this article (10.1186/s12862-019-1377-4) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Selection shapes turnover and magnitude of sex-biased expression in Drosophila gonads

Whittle

Extavour

2019

BMC Evol Biol

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“…Moreover, these flies exhibit the most extreme interspecies range of ovariole number reported in the genus, ranging from two to 101 per female [2]. Hawaiian Drosophila have undergone rapid island radiation from a common ancestor in the past 25 million years, leading to approximately 1,000 extant species [17,18]. Most of the species diversity of Hawaiian Drosophila is spread across five monophyletic species groups that share genetic, morphological, and ecological similarities and rely on different oviposition substrates [18][19][20][21], as follows (Figure 1): Scaptomyza are small species that lay eggs on leaves, flowers, and fruits, and only approximately one third of Scaptomyza species are reported to be generalists.…”

Section: Larval Ecology Influences Ovariole Number Evolutionmentioning

confidence: 99%

Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila

et al. 2019

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“…Fruit flies of the genus Drosophila including Drosophila , Sophophora , and Hawaiian Drosophila ( O’Grady and DeSalle, 2018b ) commonly live on fruits that serve as a site for feeding, mating, oviposition, and development. Usually, despite of the common macrohabitat, i.e., orchards, Drosophila flies of different species may occupy their specific microhabitats and largely avoid each other in time and space ( Mitsui et al, 2006 ; Beltrami et al, 2012 ; O’Grady and DeSalle, 2018a ; Plantamp et al, 2019 ). Some species such as Drosophila suzukii prefer, for instance, immature fruits ( Lee et al, 2011 ; Walsh et al, 2011 ; Silva-Soares et al, 2017 ; Olazcuaga et al, 2019 ), while others like Drosophila melanogaster prefer rotten fruits ( Versace et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Transcriptional Control of Quality Differences in the Lipid-Based Cuticle Barrier in Drosophila suzukii and Drosophila melanogaster

et al. 2020

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Cuticle barrier efficiency in insects depends largely on cuticular lipids. To learn about the evolution of cuticle barrier function, we compared the basic properties of the cuticle inward and outward barrier function in adults of the fruit flies Drosophila suzukii and Drosophila melanogaster that live on fruits sharing a similar habitat. At low air humidity, D. suzukii flies desiccate faster than D. melanogaster flies. We observed a general trend indicating that in this respect males are less robust than females in both species. Xenobiotics penetration occurs at lower temperatures in D. suzukii than in D. melanogaster. Likewise, D. suzukii flies are more susceptible to contact insecticides than D. melanogaster flies. Thus, both the inward and outward barriers of D. suzukii are less efficient. Consistently, D. suzukii flies have less cuticular hydrocarbons (CHC) that participate as key components of the cuticle barrier. Especially, the relative amounts of branched and desaturated CHCs, known to enhance desiccation resistance, show reduced levels in D. suzukii. Moreover, the expression of snustorr (snu) that encodes an ABC transporter involved in barrier construction and CHC externalization, is strongly suppressed in D. suzukii. Hence, species-specific genetic programs regulate the quality of the lipid-based cuticle barrier in these two Drosophilae. Together, we conclude that the weaker inward and outward barriers of D. suzukii may be partly explained by differences in CHC composition and by a reduced Snu-dependent transport rate of CHCs to the surface. In turn, this suggests that snu is an ecologically adjustable and therefore relevant gene in cuticle barrier efficiency.

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Hawaiian Drosophila as an Evolutionary Model Clade: Days of Future Past

Cited by 18 publications

References 101 publications

Selection shapes turnover and magnitude of sex-biased expression in Drosophila gonads

Selection shapes turnover and magnitude of sex-biased expression in Drosophila gonads

Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila

Transcriptional Control of Quality Differences in the Lipid-Based Cuticle Barrier in Drosophila suzukii and Drosophila melanogaster

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