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. 2020 Feb 21:9:e53237.
doi: 10.7554/eLife.53237.

Rapid sex-specific adaptation to high temperature in Drosophila

Sheng-Kai Hsu  1   2 , Ana Marija Jakšić  1   2 , Viola Nolte  1 , Manolis Lirakis  1   2 , Robert Kofler  1 , Neda Barghi  1 , Elisabetta Versace  3 , Christian Schlötterer  1
Affiliations

Rapid sex-specific adaptation to high temperature in Drosophila

Sheng-Kai Hsu et al. Elife. .

Abstract

The pervasive occurrence of sexual dimorphism demonstrates different adaptive strategies of males and females. While different reproductive strategies of the two sexes are well-characterized, very little is known about differential functional requirements of males and females in their natural habitats. Here, we study the impact environmental change on the selection response in both sexes. Exposing replicated Drosophila populations to a novel temperature regime, we demonstrate sex-specific changes in gene expression, metabolic and behavioral phenotypes in less than 100 generations. This indicates not only different functional requirements of both sexes in the new environment but also rapid sex-specific adaptation. Supported by computer simulations we propose that altered sex-biased gene regulation from standing genetic variation, rather than new mutations, is the driver of rapid sex-specific adaptation. Our discovery of environmentally driven divergent functional requirements of males and females has important implications-possibly even for gender aware medical treatments.

Keywords: Drosophila simulans; evolutionary biology; experimental evolution; genetics; genomics; sex-specific adaptation; sexual dimorphism.

Plain language summary

Male and female animals of the same species sometimes differ in appearance and sexual behavior, a phenomenon known as sexual dimorphism. Both sexes share most of the same genes, but differences can emerge because of the way these are read by cells to create proteins – a process called gene expression. For instance, certain genes can be more expressed in males than in females, and vice-versa. Most studies into the emergence of sexual dimorphism have taken place in stable environments with few changes in climate or other factors. Therefore, the potential impact of environmental changes on sexual dimorphism has been largely overlooked. Here, Hsu et al. used genetic and computational approaches to investigate whether male and female fruit flies adapt differently to a new, hotter environment over several generations. The experiment showed that, after only 100 generations, the way that 60% of all genes were expressed evolved in a different direction in the two sexes. This led to differences in how the males and females made and broke down fat molecules, and in how their neurons operated. These expression changes also translated in differences for high-level biological processes. For instance, animals in the new settings ended up behaving differently, with the males at the end of the experiment spending more time chasing females than the ancestral flies. These findings demonstrate that male and female fruit flies adapt many biological processes (including metabolism and behaviors) differently to cope with changes in their environment, and that many different genes support these sex-specific adaptations. Ultimately, the work by Hsu et al. may inform medical strategies that take into account interactions between the patient’s sex and their environment.

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Conflict of interest statement

SH, AJ, VN, ML, RK, NB, EV, CS No competing interests declared

Figures

Figure 1.
Figure 1.. Sex-specific gene expression evolution adapting to a high temperature.
(a) Evolution of gene expression in females (x axis) and males (y axis). The evolutionary changes of all expressed genes are shown on log2 scale. Genes showing different patterns of evolution are highlighted in different colors. (b) The majority of the genes with significant expression changes is sex-specific. Venn diagram showing the number of genes with significantly different gene expression patterns (DE: Differential Expression; M.up/F.up: males/females evolved higher gene expression, M.down/F.down: males/females evolved lower gene expression). (c) Genes with evolved expression changes in males and females are involved in nearly mutually exclusive sets of biological processes. Venn diagram of sets of GO (Gene ontology: biological processes) terms enriched by the genes changing their expression for each direction in each sex (i.e. four sets of candidate genes: up/down-regulation in males/females). For instance, there are only three biological processes repeatedly found among the 90 and 53 processes involving up-regulated genes in males and females respectively. (d) The tissue enrichment of genes significantly evolving for either direction in males and females (Br-brain, Hd-head, Cr-crop, Mg-midgut, Hg-hindgut, Tb-malpighian tubule, Tg-thoracoabdominal ganglion, Cs-carcass, Sg-salivary gland, Fb-fat body, Ey-eye and Hr-heart). Each cell represents the result of a Fisher’s exact test. The colors and numbers denote the magnitude of odds ratio and statistical significance (FDR < 0.05) is indicated with *. Consistent with GO enrichment results, gene expression evolution in males and females may occur in different tissues.
Figure 1—figure supplement 1.
Figure 1—figure supplement 1.. Parallel responses of adaptive genes across replicates.
Normalized expression of significant genes identified in males (A) and females (B). The heat color indicates the expression of each gene in each sample. Comparing ancestral samples (B01–B05) to each of the evolved samples (H01–H10), 91% and 87% of the candidate genes in males and females change their expression to the same direction in all replicates, respectively.
Figure 1—figure supplement 2.
Figure 1—figure supplement 2.. Evolution of sexual dimorphism.
During the adaptation to the hot laboratory environment, 673 ancestrally unbiased genes evolved to exhibit significant expression dimorphism after 100 generations. Meanwhile, 136 genes evolved for a reduction in their sexual dimorphism. Sexual dimorphism can be dynamic when the underlying sex-specific fitness landscapes change over time. Selection on the standing genetic variation in the sex-biased regulatory architecture would tune the gain and loss of sexual dimorphism.
Figure 2.
Figure 2.. Sex-specific phenotypic evolution.
(a and c) Genes involved in fatty acid metabolism and monoaminergic neural signaling evolve in response to high temperature. The evolutionary changes in males (blue bar) and females (red bar) are shown on log2 scale. Statistical significance (FDR < 0.05) is indicated with *. For both set of genes, the evolution is largely sex-specific or even sexually discordant. (b) Level of triglycerides, the main constituent of body fat data from Barghi et al. (2019). Evolved females have significantly lower fat content than the ancestral ones. No significant difference is found in males. Two-way ANOVA and Tuckey’s HSD test. (d) Ovarian dormancy incidence at 10°C in ancestral and evolved females. Evolved females have a lower dormancy incidence than ancestral ones (Wilcoxon’s test, W = 1.5, p=0.028). (e) Time males chasing females. Evolved males spent significantly more time chasing females (Wilcoxon’s test, W = 1323.5, p<0.001).
Figure 2—figure supplement 1.
Figure 2—figure supplement 1.. Ovarian dormancy incidence at 12°C.
Evolved females have a lower dormancy incidence than ancestral ones (Wilcoxon’s test, W = 3.5, p=0.061).
Figure 2—figure supplement 2.
Figure 2—figure supplement 2.. Time male flies attempting to copulate.
Evolved males spent significantly more time chasing females (Wilcoxon’s test, W = 1174, p<0.001).
Figure 3.
Figure 3.. A simple model for rapid evolution of sex-specific adaptation.
Regulatory variation segregating at a transcription factor is selected for a more pronounced difference in gene expression between sexes. This also causes more pronounced expression differences in a downstream gene satisfying the altered requirements of the two sexes in the new environment. (A) Regulatory cascade of a transcription factor (TF) controlled by sex-specific isoforms of Dsx. Two alleles with different binding affinity (B > b) with DsxM but not with DsxF are regulating downstream genes affecting fitness (FG). (B) Frequency of the allele increasing sex bias (B allele) at three different stages: in the native (natural) environment, in the new hot environment at the start of the experiment, in the new hot environment at the end of the experiment. (C) Fitness landscape at the three different stages. (D) Expression of TF and FG in males and females at the different stages. After 100 generations, the frequency increase of the allele increasing sex-biased expression of the TF results in a resolved intra-locus conflict.
Figure 4.
Figure 4.. Rapid decoupling of the phenotypic response to sexually discordant trait optima by a few sex-specific loci.
(a) The phenotypic response of a trait controlled by 50 loci after 100 generations of sexually discordant selection. Different numbers of sex-specific loci in each sex are shown. For each scenario, 100 independent computer simulations were performed. The normalized phenotypic change is calculated as the ratio between phenotypic change and phenotypic variance of the ancestral population. (b) Fraction of simulations for which the focal trait increases in males but decreases in females. The statistical significance denoted by an asterisk is based on one-sample proportion test comparing to the control simulation without any sex-specific locus. Bonferroni’s correction is applied. Already two sex-specific loci in each sex significantly decouples the phenotypic responses to the discordant selection. With increasing numbers of sex-specific loci, the difference between the sex-specific phenotypic responses becomes more pronounced.
Figure 4—figure supplement 1.
Figure 4—figure supplement 1.. Sex-specific responses to discordant selection via sex-biased loci.
(a) The phenotypic response of a trait controlled by 50 loci after 100 generations of sexually discordant selection. Different numbers of sex-biased loci in each sex are shown. For each scenario, 100 independent computer simulations were performed. The normalized phenotypic change is calculated as the ratio between phenotypic change and phenotypic variance of the ancestral population. (b) Fraction of simulations in which there’s a simultaneous increase in male but decrease in females of the focal trait. The statistical significance denoted by ‘*” is based on one-sample proportion test comparing to the control simulation without any sex-biased locus. Bonferroni’s correction is applied.
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