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Spatiotemporal dynamics and genome-wide association genome-wide association analysis of desiccation tolerance in Drosophila melanogaster - PubMed

. 2018 Sep;27(17):3525-3540.

doi: 10.1111/mec.14814. Epub 2018 Aug 13.

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Spatiotemporal dynamics and genome-wide association genome-wide association analysis of desiccation tolerance in Drosophila melanogaster

Subhash Rajpurohit et al. Mol Ecol. 2018 Sep.

Abstract

Water availability is a major environmental challenge to a variety of terrestrial organisms. In insects, desiccation tolerance varies predictably over spatial and temporal scales and is an important physiological determinant of fitness in natural populations. Here, we examine the dynamics of desiccation tolerance in North American populations of Drosophila melanogaster using: (a) natural populations sampled across latitudes and seasons; (b) experimental evolution in field mesocosms over seasonal time; (c) genome-wide associations to identify SNPs/genes associated with variation for desiccation tolerance; and (d) subsequent analysis of patterns of clinal/seasonal enrichment in existing pooled sequencing data of populations sampled in both North America and Australia. A cline in desiccation tolerance was observed, for which tolerance exhibited a positive association with latitude; tolerance also varied predictably with culture temperature, demonstrating a significant degree of thermal plasticity. Desiccation tolerance evolved rapidly in field mesocosms, although only males showed differences in desiccation tolerance between spring and autumn collections from natural populations. Water loss rates did not vary significantly among latitudinal or seasonal populations; however, changes in metabolic rates during prolonged exposure to dry conditions are consistent with increased tolerance in higher latitude populations. Genome-wide associations in a panel of inbred lines identified twenty-five SNPs in twenty-one loci associated with sex-averaged desiccation tolerance, but there is no robust signal of spatially varying selection on genes associated with desiccation tolerance. Together, our results suggest that desiccation tolerance is a complex and important fitness component that evolves rapidly and predictably in natural populations.

Keywords: Drosophila; cline; desiccation tolerance; plasticity; season.

© 2018 John Wiley & Sons Ltd.

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Figures

Figure 1:
Figure 1:

Temperature map of the east coast of the U.S. showing the populations of D. melanogaster that were collected and assayed. Collection sites for the latitudinal & seasonal populations are shown in white stars and black dots respectively. Bowdoin, Maine (ME); Lancaster, Massachusetts (MA); Media, Pennsylvania (PA); Charlottesville, Virginia (VA); Athens, Georgia (GA); Jacksonville, Florida (JFL), Homestead, Florida (HFL).

Figure 2:
Figure 2:

Data on desiccation tolerance for males and females of D. melanogaster from six geographical locations (see Fig. 1) at four different thermal conditions (developmental temperatures of 18 °C, 25 °C, and 29 °C; adult female exposure to dormancy-inducing conditions of 11˚C, 9L:15D). Data are presented as LT50 means. Males and females are denoted as triangles and rectangles, respectively. r = correlation; b = slope. Analysis of developmental temperature is presented in Table 1; for the reproductive dormancy treatment for adult females, latitude is a significant predictor of tolerance (F10,75, df=5, SS=269.99, p < 10−6).

Figure 3:
Figure 3:

Data (mean ± s.e) on early and late season desiccation tolerance for males and females of D. melanogaster from three geographical locations (Lancaster, MA; Media, PA; Charlottesville, VA). Open, gray and black bars represent MA, PA and VA populations, respectively. The effect of season is significant for males only, and is driven by differences between spring and fall collections in the Media, PA population.

Figure 4:
Figure 4:

Rapid evolution of desiccation tolerance in field mesocosms. (A) Mean temperature and RH across the 10 replicate mesocosms are plotted over the duration of the experiment. (B) Mean (± s.e.m.) desiccation tolerance for females (closed symbols) and males (open symbols) at the four sampling time points in 2014. Tolerance increased for both females and males from July 25 to August 19 (F1,2357 = 339.91, p < 0.0001; F1,2358 = 9.63, p < 0.002, respectively). Over the period from September 11 to October 10, tolerance decreased in females (F1,2357 = 11.59, p < 0.001) and increased in males (F1,2357 = 41.44, p < 0.0001).

Figure 5:
Figure 5:

Carbon dioxide emission rates for males (A) and females (B) of D. melanogaster populations from Florida (HFL) and Maine (ME). Measurements were done at two time points (30 min and 3hr). Asterisks indicate a significant difference between measurements conducted at the two timepoints (α=0.05). Within population differences (for FL males and ME females) measured at two-time points (30min and 3hr) are shown with dashed line connections. The differences at the population level are shown with the solid lines connections. After 3h, FL males have higher values than ME males. In comparing FL males 30min to 3h treatment, there is a significant increase in VCO2. In females, ME flies show a decrease in VCO2 going from 30min to 3hr.

Figure 6:
Figure 6:

Status of desiccation tolerance (line means) in Drosophila Genetic Resource Panel. A total of 175 lines were considered for this association mapping. A considerable genetic variability in desiccation tolerance was observed across the lines. Males (A) survived shorter under desiccating conditions than females (B). Desiccation tolerance values are sorted in increasing order for males in panel A, and corresponding lines values for females are shown in panel B. The data show extensive within-line differences between the sexes, consistent with the differential response in the field mesocosms (Fig. 4).

Figure 7:
Figure 7:

Signals of clinality among North American and Australian populations at genes associated with desiccation tolerance. (A) and (C) represent SumStat scores for 5000 sets of control genes (distribution) and observed SumStat score (dashed red line) for genes associated with desiccation tolerance among populations sampled along the east coast of North America or Australia, respectively. (B) and (D) represent per-gene probabilities that the observed zst(g) values are bigger than expected by chance for North American and Australian populations, respectively. See Materials and Methods for a description of the SumStat score.

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