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A Rapid Shift in a Classic Clinal Pattern in Drosophila Reflecting Climate Change

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Science  29 Apr 2005:
Vol. 308, Issue 5722, pp. 691-693
DOI: 10.1126/science.1109523

Abstract

Geographical clines in genetic polymorphisms are widely used as evidence of climatic selection and are expected to shift with climate change. We show that the classic latitudinal cline in the alcohol dehydrogenase polymorphism of Drosophila melanogaster has shifted over 20 years in eastern coastal Australia. Southern high-latitude populations now have the genetic constitution of more northerly populations, equivalent to a shift of 4° in latitude. A similar shift was detected for a genetically independent inversion polymorphism, whereas two other linked polymorphisms exhibiting weaker clinal patterns have remained relatively stable. These genetic changes are likely to reflect increasingly warmer and drier conditions and may serve as sensitive biomarkers for climate change.

Clinal variation in genetic polymorphisms and traits occurs in natural populations of numerous species. Such variation provides strong evidence of natural selection and adaptation to different environmental variables, particularly climatic conditions (1). Perhaps the most compelling evidence for climatic selection generating clinal patterns comes from the many studies on latitudinal clinal variation in Drosophila melanogaster. This cosmopolitan species is closely associated with human activities, and its abundance is typically high in farmed areas and in decaying fruit and vegetable matter. Latitudinal clines have been shown in D. melanogaster for traits such as body size, development time, and thermal resistance (24) and for various genetic markers at the allele and karyotype level (58).

The alcohol dehydrogenase (Adh) locus in this species is one of the most thoroughly studied examples of a genetic latitudinal cline in any organism, with the AdhS allele increasing in frequency with decreasing latitude in both the Northern and Southern hemispheres (5, 9, 10). Temperature-related factors influence population allele frequencies both in the field (6, 11) and in the laboratory (12, 13); rainfall and humidity levels have also been implicated (5).

Using molecular markers for Adh (14), we recharacterized the D. melanogaster cline along coastal eastern Australia in 2002 and 2004 and compared the results to data from earlier studies (5, 15) that involved collections in 1979 and 1982. The combined data set from these different periods showed a significant difference in elevation but not in the slope of the regression lines (Fig. 1 and Table 1), with elevation shifting in the direction expected with rising temperatures and global warming (6, 16). Because the AdhS allele that predominates in tropical populations is now at a higher frequency in all populations, there has been a tendency for populations to evolve toward the genetic composition of lower latitude populations. Conversely, we found no differences in either line slope (t = 1.164, df = 30, P = 0.254) or line elevation (t = 0.842, df = 31, P = 0.406) between the 2002 and 2004 collections. Nor did we find any differences in slope (t = 0.973, df = 42, P = 0.336) or elevation (t = 0.305, df = 43, P = 0.762) between the 1979 and 1982 collections.

Fig. 1.

Change in latitudinal patterns, between 1979 and 1982 and between 2002 and 2004, of the frequencies of the S allele of alcohol dehydrogenase (AdhS), the inversions In(3R)Payne and In(2L)t, and the F allele of sn-glycerol-3-phosphate dehydrogenase (α-GpdhF). Open symbols and dashed lines indicate 1979–1982 pooled data points (except α-GpdhF where only 1979 data were available); solid symbols and solid lines indicate 2002–2004 pooled data.

Table 1.

Linear regressions examining associations between markers and latitude in 1979–1982 and 2002–2004 collections of D. melanogaster from the east coast of Australia. Probability tests for differences between slopes and elevations of the regression equations are also provided.

Marker Year Regression equation R2tpp values for comparison of two collections
Slope Elevation
AdhS 2002-2004 y = -0.028x + 1.794 0.899 16.873 <0.001 0.677 <0.001
1979-1982 y = -0.026x + 1.651 0.664 9.314 <0.001
In(2L)t 2002-2004 y = -0.018x + 0.982 0.551 6.272 <0.001 0.480 0.079
1979-1982 y = -0.020x + 1.009 0.652 9.077 <0.001
In(3R)Payne 2002-2004 y = -0.033x + 1.797 0.772 10.413 <0.001 0.586<0.001
1979-1982 y = -0.035x + 1.619 0.696 10.047 <0.001

In studies of latitudinal transects, the AdhS allele has been positively associated with In(2L)t, a cosmopolitan inversion that also clines latitudinally (6, 7). Adh is located just outside the proximal breakpoint of this inversion, whereas α-Gpdh, the gene encoding another commonly studied cytosolic enzyme (sn-glycerol-3-phosphate dehydrogenase), is inside it; in natural populations, this locus is usually in disequilibrium with the inversion. We examined changes in patterns at both the α-Gpdh locus (14) and for In(2L)t, again pooling across years on the basis of nonsignificant changes in slope and elevation. In the earlier studies (7, 15), In(2L)t had been scored cytologically after laboratory culture of lines, but we used a molecular marker to score this inversion directly on field flies, following Andolfatto et al. (14, 17). The 1979–1982 and 2002–2004 data for In(2L)t did not differ significantly in terms of either the slope or elevation of the regression lines (Fig. 1 and Table 1), although there was a nonsignificant trend in the same direction to that observed for Adh. Although a weak latitudinal cline has been suggested previously for α-Gpdh in Australia (5, 18), we found no significant linear association between α-Gpdh and latitude in the 2002 (t = 0.945, P = 0.361) and 2004 (t = 1.675, P = 0.113) collections (Fig. 1). Furthermore, there was no significant difference in the mean frequency of α-Gpdh between the 1979 and the pooled 2002–2004 populations (t = –1.764, df = 53, P = 0.084). Therefore, despite the genetic and possible adaptive interdependence of α-Gpdh and In(2L)t with Adh, they have remained relatively unchanged in latitudinal position.

We estimated the magnitude of the shift in elevation of the clinal pattern for the Adh polymorphism, as well as for a common cosmopolitan inversion on a different chromosome, In(3R)Payne, which also clines with latitude and has shifted in elevation (but not slope) in the past 20 years (19) (Fig. 1 and Table 1). For Adh, the shift corresponded to 3.9° in latitude [bootstrap 95% confidence limits (CLs) of 2.01 and 5.92], equivalent to more than 400 km. For In(3R)Payne the shift was larger, at 7.3° in latitude (CLs of 4.85 and 10.51), corresponding to a shift of more than 800 km.

What factors might be responsible for these latitudinal shifts? Adh frequencies have previously been related to temperature and rainfall (5, 11, 16), and because these factors vary clinally, they are likely contenders. The climate along the eastern coast of Australia is gradually becoming warmer and drier, and recent evidence shows that over the past 50 years these changes have increased markedly as a result of human activities (20, 21). Mean temperature is increasing at most coastal locations at a rate of 0.1° to 0.3°C every 10 years, whereas rainfall is decreasing at a rate of 10 to 70 mm per year. These changes are also evident in a comparison of data from weather stations along the eastern coast of Australia covering the area sampled for the molecular markers. Average differences between 1978 and 1981 and between 2000 and 2003 (1 to 2 years before each set of collections) were compared for 36 weather stations along the eastern coast at low altitudes (<50 m) on the basis of data from the Australian Bureau of Meteorology (22). There were significant differences (using paired t tests) between years in 11 of the 15 climatic variables considered. When data for four of these variables—change in mean daily maximum temperature of the coldest month (t = 4.288, df = 35, P < 0.001), change in average daily maximum temperature (t = 7.218, df = 35, P = 0.001), change in mean daily humidity at 9 a.m. (t = –4.918, df = 29, P = 0.001), and change in total annual rainfall (t = –2.437, df = 28, P = 0.021)—are plotted against latitude, they indicate higher mean daily maximum temperatures, lower humidity, and a decrease in rainfall at most latitudes (Fig. 2).

Fig. 2.

Differences between 1979–1982 and 2002–2004 values for four climatic variables plotted against latitude. Positive values indicate higher scores for 2002–2004.

Combinations of climatic variables are likely to provide the best indicators of the shifts in genetic constitution, because changes in any one of these single climatic variables do not appear to account for the extent of the latitudinal shift observed. For instance, the 0.66°C shift in the maximum daily temperature of the coldest month across samples amounts to a shift in latitude of only 1.3°, which is outside the lower bootstrap confidence intervals of the shifts estimated for both Adh and In(3R)Payne. The combined effect of different climatic factors may underlie the changed environment that has driven the coastal shift in AdhS and In(3R)Payne frequencies.

Climatically driven changes in the genetic constitution of D. melanogaster populations are not entirely unexpected, because climate-associated changes in chromosomal inversions have been documented for the Drosophila species D. robusta (23) and D. subobscura (24). In addition, previous Drosophila field studies suggest that changes in frequencies of inversions and single-gene alleles can occur rapidly (25) as well as seasonally (26, 27). On the basis of distribution records, it is thought that D. melanogaster first entered Australia from the north about 100 years ago (28). Despite the relative recency of this introduction and molecular data indicating a high rate of gene flow (29), clinal variation is well established for several traits and several genetic polymophisms along the Australian eastern coast (3, 30). Therefore, the genetic shift documented here is unlikely to be the tail end of adaptation to a temporally stable environmental transect by an introduced species; instead, it may be part of a rapid genetic response of a species to climate change, as has recently been suggested for an adaptive trait in another insect species (31).

The Adh enzyme polymorphism in D. melanogaster and the common cosmopolitan inversions in this species are valuable examples of clinal variation along latitudinal gradients, resulting in genetic constitutions appropriate to local climatic conditions. The shift in polymorphisms with climatic change indicates how Adh [and potentially In(3R)Payne] can be linked to the dynamics of adaptive processes. We have shown that adaptive polymorphisms could provide monitoring tools for detecting the impact of climate change on populations.

Supporting Online Material

www.sciencemag.org/cgi/content/full/308/5722/691/DC1

Materials and Methods

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