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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 degrees 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.
A Rapid Shift in a Classic
Clinal Pattern in Drosophila
Reflecting Climate Change
P. A. Umina,
A. R. Weeks,
M. R. Kearney,
S. W. McKechnie,
A. A. Hoffmann
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 Aus-
tralia. Southern high-latitude populations now have the genetic constitution
of more northerly populations, equivalent to a shift of 4- in latitude. A simi-
lar 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 numer-
ous species. Such variation provides strong
evidence of natural selection and adaptation
to different environmental variables, particu-
larly 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 ac-
tivities, and its abundance is typically high in
farmed areas and in decaying fruit and veg-
etable matter. Latitudinal clines have been
shown in D. melanogaster for traits such as
body size, development time, and thermal re-
sistance (2–4) and for various genetic markers
at the allele and karyotype level (5–8).
The alcohol dehydrogenase (Adh) locus
in this species is one of the most thorough-
ly studied examples of a genetic latitudinal
cline in any organism, with the Adh
increasing in frequency with decreasing lat-
itude in both the Northern and Southern hemi-
spheres (5, 9, 10). Temperature-related fac-
tors 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 Adh
allele that predominates
in tropical populations is now at a higher fre-
quency in all populations, there has been a
tendency for populations to evolve toward the
genetic composition of lower latitude popula-
tions. Conversely, we found no differences in
either line slope (t 0 1.164, df 0 30, P 0 0.254)
or line elevation (t 0 0.842, df 0 31, P 0 0.406)
between the 2002 and 2004 collections. Nor
did we find any differences in slope (t 0 0.973,
df 0 42, P 0 0.336) or elevation (t 0 0.305,
df 0 43, P 0 0.762) between the 1979 and
1982 collections.
In studies of latitudinal transects, the Adh
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 inver-
sion, whereas a-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 a-Gpdh locus (14)andforIn(2L)t,again
pooling across years on the basis of nonsig-
nificant 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
Centre for Environmental Stress and Adaptation
Research, School of Biological Sciences, Monash
University, Clayton, Victoria 3800, Australia.
for Environmental Stress and Adaptation Research, La
Trobe University, Bundoora, Victoria 3086, Australia.
*To whom correspondence should be addressed.
Fig. 1. Change in latitudinal
patterns, between 1979 and
1982 and between 2002 and
2004, of the frequencies of
the S allele of alcohol dehy-
drogenase (Adh
), the inver-
sions In(3R)Payne and In(2L)t,
and the F allele of sn-glycerol-
3-phosphate dehydrogenase
). Open symbols and
dashed lines indicate 1979–
1982 pooled data points (ex-
cept a-Gpdh
where only
1979 data were available);
solid symbols and solid lines
indicate 2002–2004 pooled
15 20 25 30 35 40 45
fr ycneuqe
15 20 25 30 35 40 45
R f
15 20 25 30 35 40 45
15 20 25 30 35 40 45
Latitude (de
rees South)
1979/1982 - - - -
score this inversion directly on field flies, fol-
lowing 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 a-Gpdh in Aus-
tralia (5, 18), we found no significant linear
association between a-Gpdh and latitude in
the 2002 (t 0 0.945, P 0 0.361) and 2004 (t 0
1.675, P 0 0.113) collections (Fig. 1). Further-
more, there was no significant difference in the
mean frequency of a-Gpdh between the 1979
and the pooled 2002–2004 populations (t 0
–1.764, df 0 53, P 0 0.084). Therefore, de-
spite the genetic and possible adaptive inter-
dependence of a-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 cosmo-
politan 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
Ebootstrap 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), correspond-
ing to a shift of more than 800 km.
What factors might be responsible for these
latitudinal shifts? Adh frequencies have previ-
ously been related to temperature and rainfall
(5, 11, 16), and because these factors vary cli-
nally, they are likely contenders. The climate
along the eastern coast of Australia is grad-
ually becoming warmer and drier, and re-
cent 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 be-
tween 1978 and 1981 and between 2000 and
2003 (1 to 2 years before each set of collec-
tions) were compared for 36 weather stations
along the eastern coast at low altitudes (G50 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 0 4.288, df 0 35, P G 0.001),
change in average daily maximum tempera-
ture (t 0 7.218, df 0 35, P G 0.001), change
in mean daily humidity at 9 a.m. (t 0 –4.918,
df 0 29, P G 0.001), and change in total an-
nual rainfall (t 0 –2.437, df 0 28, P 0 0.021)—
are plotted against latitude, they indicate high-
er mean daily maximum temperatures, lower
humidity, and a decrease in rainfall at most
latitudes (Fig. 2).
Combinations of climatic variables are like-
ly 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 temper-
ature of the coldest month across samples
amounts to a shift in latitude of only 1.3-,
which is outside the lower bootstrap confi-
dence 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 coast-
al shift in Adh
and In(3R)Payne frequencies.
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
P values for comparison
of two collections
Slope Elevation
2002–2004 y 0 –0.028x þ 1.794 0.899 16.873 G0.001
0.677 G0.001
1979–1982 y 0 –0.026x þ 1.651 0.664 9.314 G0.001
In(2L)t 2002–2004 y 0 –0.018x þ 0.982 0.551 6.272 G0.001
0.480 0.079
1979–1982 y 0 –0.020x þ 1.009 0.652 9.077 G0.001
In(3R)Payne 2002–2004 y 0 –0.033x þ 1.797 0.772 10.413 G0.001
0.586 G0.001
1979–1982 y 0 –0.035x þ 1.619 0.696 10.047 G0.001
Fig. 2. Differences between
1979–1982 and 2002–2004
variables plotted against
latitude. Positive values
indicate higher scores for
Mean maximum daily temperature
20 25 30 35 40 45
gnae(d egr ees )C
Mean daily 9 am humidity
20 25 30 35 40 45
itidychnaeg( pnp
Total annual rainfall
20 25 30 35 40 45
Latitude (degrees South)
fniaRallc eg
Mean maximum daily temperature of coldest month
20 25 30 35 40 45
Temp reaturecha egn( dgereesC )
Climatically driven changes in the genetic
constitution of D. melanogaster populations
are not entirely unexpected, because climate-
associated changes in chromosomal inver-
sions have been documented for the Drosophila
species D. robusta (23)andD. subobscura (24).
In addition, previous Drosophila field studies
suggest that changes in frequencies of inver-
sions and single-gene alleles can occur rapidly
(25)aswellasseasonally(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 poly-
mophisms along the Australian eastern coast
(3, 30). Therefore, the genetic shift document-
ed here is unlikely to be the tail end of adap-
tation 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 an-
other insect species (31).
The Adh enzyme polymorphism in D. mel-
anogaster and the common cosmopolitan in-
versions in this species are valuable examples
of clinal variation along latitudinal gradients,
resulting in genetic constitutions appropriate
to local climatic conditions. The shift in poly-
morphisms with climatic change indicates how
Adh Eand 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.
References and Notes
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Australian Research Council postdoctoral fellowships.
Supporting Online Material
Materials and Methods
7 January 2005; accepted 9 February 2005
PERIOD1-Associated Proteins
Modulate the Negative Limb of the
Mammalian Circadian Oscillator
Steven A. Brown,
Juergen Ripperger,
Sebastian Kadener,
Fabienne Fleury-Olela,
Francis Vilbois,
Michael Rosbash,
Ueli Schibler
The clock proteins PERIOD1 (PER1) and PERIOD2 (PER2) play essential roles in
a negative transcriptional feedback loop that generates circadian rhythms in
mammalian cells. We identified two PER1-associated factors, NONO and
WDR5, that modulate PER activity. The reduction of NONO expression by
RNA interference (RNAi) attenuated circadian rhythms in mammalian cells,
and fruit flies carrying a hypomorphic allele were nearly arrhythmic. WDR5, a
subunit of histone methyltransferase complexes, augmented PER-mediated
transcriptional repression, and its reduction by RNAi diminished circadian
histone methylations at the promoter of a clock gene.
About 10% of all mammalian transcripts show
daily oscillations of abundance (1). These rhyth-
mic fluctuations are governed by a molecular
circadian clock, whose function relies on two
interconnected feedback loops of transcription.
In the major negative feedback loop, tran-
scription of the Period (Per1 and Per2)and
Cryptochrome (Cry1 and Cry2) genes, and of
Rev-Erba, an orphan nuclear receptor gene, is
activated by the transcription factors CLOCK
teins themselves (2). Although PERs interact
with CRYs (3), the mechanism by which they
repress CLOCK:BMAL1–mediated clock gene
transcription remains poorly understood.
To elucidate the sizes of the PER1 and PER2
complexes involved in this process, we fraction-
ated nuclear extracts of mouse livers by gel
filtration chromatography. During the night,
the two proteins formed similarly large com-
plexes (91 MD) (Fig. 1A), whose abundance
and size distribution changed during the day
(fig. S1). Thus, PERs associate with other pro-
teins that may play roles in the function of
the circadian oscillator. To identify them, we
generated a Rat-1 fibroblast cell line that ex-
presses a PER1 protein containing a 6xHis tag
and a V5 epitope tag at its C terminus. The ex-
pression of a His-V5-PER1 protein was three
times higher than that of endogenous PER1 in
unsynchronized cells (Fig. 1B, lanes 1 and 2)
and did not interfere with the circadian tran-
scription of other clock or clock-controlled
genes (4).
Nuclear extracts from His-V5-PER1 cells
were harvested 3 hours after the induction of
circadian rhythms by serum treatment. Because
clock-controlled genes such as Dbp and Rev-
erba arerepressedduringthistimeperiod(5),
PER-mediated transcriptional repression would
likely be operative as well. After chromatogra-
phy of this extract was performed on nickel
Department of Molecular Biology and National
Centres of Competence in Research (NCCR) Frontiers
in Genetics, Sciences III, University of Geneva, 30 Quai
Ernest Ansermet, CH-1211 Geneva-4, Switzerland.
Department of Biology, Howard Hughes Medical
Institute, Brandeis University, Waltham, MA 02454,
Serono Pharmaceutical Research Institute, 14
Chemin des Aulx, 1228 Plan-les-Ouates, Geneva,
*To whom correspondence should be addressed.
E-mail: (S.A.B.); Ueli. (U.S.)
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In all species, new chromosomal inversions are constantly being formed by spontaneous rearrangement and then stochastically eliminated from natural populations. In Drosophila, when new chromosomal inversions overlap with a pre-existing inversion in the population, their rate of elimination becomes a function of the relative size, position, and linkage phase of the gene rearrangements. These altered dynamics result from complex meiotic behavior wherein overlapping inversions generate asymmetric dyads that cause both meiotic drive/drag and segmental aneuploidy. In this context, patterns in rare inversion polymorphisms of a natural population can be modeled from the fundamental genetic processes of forming asymmetric dyads via crossing-over in meiosis I and preferential segregation from asymmetric dyads in meiosis II. Here, a mathematical model of crossover-dependent female meiotic drive is developed and parameterized with published experimental data from Drosophila melanogaster laboratory constructs. This mechanism is demonstrated to favor smaller, distal inversions and accelerate the elimination of larger, proximal inversions. Simulated sampling experiments indicate that the paracentric inversions directly observed in natural population surveys of Drosophila melanogaster are a biased subset that both maximizes meiotic drive and minimizes the frequency of lethal zygotes caused by this cytogenetic mechanism. Incorporating this form of selection into a population genetic model accurately predicts the shift in relative size, position, and linkage phase for rare inversions found in this species. The model and analysis presented here suggest that this weak form of female meiotic drive is an important process influencing the genomic distribution of rare inversion polymorphisms.
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In an epoch of rapid environmental change, understanding and predicting how biodiversity will respond to a changing climate is an urgent challenge. Since we seldom have sufficient long‐term biological data to use the past to anticipate the future, spatial climate–biotic relationships are often used as a proxy for predicting biotic responses to climate change over time. These ‘space‐for‐time substitutions’ (SFTS) have become near ubiquitous in global change biology, but with different subfields largely developing methods in isolation. We review how climate‐focussed SFTS are used in four subfields of ecology and evolution, each focussed on a different type of biotic variable – population phenotypes, population genotypes, species' distributions, and ecological communities. We then examine the similarities and differences between subfields in terms of methods, limitations and opportunities. While SFTS are used for a wide range of applications, two main approaches are applied across the four subfields: spatial in situ gradient methods and transplant experiments. We find that SFTS methods share common limitations relating to ( i ) the causality of identified spatial climate–biotic relationships and ( ii ) the transferability of these relationships, i.e. whether climate–biotic relationships observed over space are equivalent to those occurring over time. Moreover, despite widespread application of SFTS in climate change research, key assumptions remain largely untested. We highlight opportunities to enhance the robustness of SFTS by addressing key assumptions and limitations, with a particular emphasis on where approaches could be shared between the four subfields.
Allele frequencies can shift rapidly within natural populations. Under certain conditions, repeated rapid allele frequency shifts can lead to the long-term maintenance of polymorphism. In recent years, studies of the model insect Drosophila melanogaster have suggested that this phenomenon is more common than previously believed and is often driven by some form of balancing selection, such as temporally fluctuating or sexually antagonistic selection. Here we discuss some of the general insights into rapid evolutionary change revealed by large-scale population genomic studies, as well as the functional and mechanistic causes of rapid adaptation uncovered by single-gene studies. As an example of the latter, we consider a regulatory polymorphism of the D. melanogaster fezzik gene. Polymorphism at this site has been maintained at intermediate frequency over an extended period of time. Regular observations from a single population over a period of 7 years revealed significant differences in the frequency of the derived allele and its variance across collections between the sexes. These patterns are highly unlikely to arise from genetic drift alone or from the action of sexually antagonistic or temporally fluctuating selection individually. Instead, the joint action of sexually antagonistic and temporally fluctuating selection can best explain the observed rapid and repeated allele frequency shifts. Temporal studies such as those reviewed here further our understanding of how rapid changes in selection can lead to the long-term maintenance of polymorphism as well as improve our knowledge of the forces driving and limiting adaptation in nature.
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Since the pioneering work of Dobzhansky in the 1930s and 1940s, many chromosomal inversions have been identified but how they contribute to adaptation remains poorly understood. In Drosophila melanogaster, the widespread inversion polymorphism In(3R)Payne underpins latitudinal clines in fitness traits on multiple continents. Here, we use single-individual whole-genome sequencing, transcriptomics and published sequencing data to study the population genomics of this inversion on four continents: in its ancestral African range and in derived populations in Europe, North America, and Australia. Our results confirm that this inversion originated in sub-Saharan Africa and subsequently became cosmopolitan; we observe marked monophyletic divergence of------- inverted and non-inverted karyotypes, with some substructure among inverted chromosomes between continents. Despite divergent evolution of this inversion since its out-of-Africa migration, derived non-African populations exhibit similar patterns of long-range linkage disequilibrium between the inversion breakpoints and major peaks of divergence in its center, consistent with balancing selection and suggesting that the inversion harbors alleles that are maintained by selection on several continents. Using RNA-seq we identify overlap between inversion-linked SNPs and loci that are differentially expressed between inverted and non-inverted chromosomes. Expression levels are higher for inverted chromosomes at low temperature, suggesting loss of buffering or compensatory plasticity and consistent with higher inversion frequency in warm climates. Our results suggest that this ancestrally tropical balanced polymorphism spread around the world and became latitudinally assorted along similar but independent climatic gradients, always being frequent in subtropical/tropical areas but rare or absent in temperate climates.
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Among Australasian populations from above 32.5 latitude there is a significant negative relationship between Gpdh F frequency and distance from the equator which is not explained by gametic disequilibrium with the linked inversion In(2L)t. This is consistent with the associations reported earlier for Gpdh F among populations covering comparable latitudes in North America and Europe/Asia. By contrast, Tpi allele frequencies are found to be significantly associated with distance from the equator in Australasia but not North America or Europe/Asia. The Tpi pattern in the different zones is essentially the same as that reported earlier for the Acph polymorphism, which maps only 0.2 cM away from the Tpi locus.There are now ten enzyme polymorphisms in D. melanogaster which have been screened for latitudinal associations in Australasia, North America and Europe/Asia. Allele frequencies at six of these loci show significant relationships with distance from the equator which are consistent across all three zones. These latitudinal associations are more prevalent for Group II than Group I enzymes. Values of genic heterozygosity averaged over the ten polymorphic loci and eleven other monomorphic systems do not vary with latitude but differ substantially between zones. Values of Nei's genetic distance between North American and European/Asian populations calculated from all 21 systems are equivalent to subspecific differences elsewhere in the genus.
The allozyme polymorphism at the alcohol dehydrogenase locus in Drosophila melanogaster was studied in order to obtain experimental evidence about the maintenance of this polymorphism. Populations started with different initial allele frequencies from homozygous F and S lines showed a convergence of frequencies on regular food at 25°, leading to values equal to those in the base populations. These results were interpreted as due to some kind of balancing selection. In populations kept at 29.8°, a lower equilibrium F frequency was attained. Addition of ethanol and some other alcohols to the food gave a rapid increase in F frequency, and high humidity decreased the F frequency slightly. Combination or alternation of ethanol and high humidity had variable effects in the populations tested. For a further analysis of the allele-frequency changes, estimates were obtained for egg-to-adult survival under different conditions and for adult survival on ethanol-supplemented food. On ethanol food (both at regular and high humidity), egg-to-adult survival of SS homozygotes was considerably lower than that of the FF and FS genotypes. Under regular conditions of food, temperature and humidity, a tendency to heterozygote superiority was observed, while at high humidity a relative high survival of SS was noticed in some tests. Adult survival of SS was lower than that of FF, but FS was generally intermediate, though the degree of dominance differed between populations. The results are consistent with the hypothesis of the occurrence of selection at the Adh locus.
In the late sixties the neo-Darwinian theory of evolution, hitherto generally accepted by biologists, was confronted with a new, revolutionary view: the theory of neutral or non-Darwinian evolution. In the neutralist view amino acid and nucleotide changes in the course of evolution are mainly due to random fixation of selectively neutral mutants (Kimura, 1968; King and Jukes, 1969). The approximately constant rate of evolution in terms of amino acid substitutions per site per year for various lineages, as claimed by neutralists, forms one of the main arguments for the neutralist theory. Enzyme polymorphisms in present-day populations are considered as a phase in molecular evolution (Kimura and Ohta, 1971; Kimura, 1977). The first estimates of the extent of enzyme polymorphisms in populations of Drosophila pseudoobscura (Lewontin and Hubby, 1966) and humans (Harris, 1966) based on electrophoresis of proteins were soon followed by many others, covering a wide range of animal and plant species. These surveys showed that most species are highly polymorphic [see reviews by Powell (1975), Nevo (1978), A. H. D. Brown (1979), and Hamrick et al. (1979)]. In the neutralist versus selectionist controversy the nature of these allozyme polymorphisms is disputed. Thw neutralist hypothesis states that the observed variation is mainly a product of mutation and drift of selectively neutral genes. The selectionist hypothesis claims that some from of balancing selection is resposible for the maintenance of allozyme polymorphisms.
In insects, species comparisons suggest a weak association between upper thermal limits and latitude in contrast to a stronger association for lower limits. To compare this to latitudinal patterns of thermal responses within species, we considered latitudinal variation in heat and cold resistance in Drosophila melanogaster. We found opposing clines in resistance to these temperature extremes in comparisons of 17–24 populations from coastal eastern Australia. Knockdown time following heat shock increased towards the tropics, whereas recovery time following cold shock decreased towards temperate latitudes. Mortality following cold shock also showed a clinal pattern. Clinal associations with latitude were linear and related to minimum temperatures in the coldest month (for cold resistance) and maximum temperatures in the warmest month (for heat resistance). This suggests that within species both high and low temperature responses can vary with latitude as a consequence of direct or indirect effects of selection.
The Adh and αGpdh allozyme loci (both located on the second chromosome) showed considerable fluctuations in allele frequencies in a seminatural population of Drosophila melanogaster during 1972–97. Both long-term and short-term fluctuations were observed. The short-term fluctuations occurred within almost all years and comparison of allele frequencies between winters and summers showed significantly higher AdhS (P < 0.001) and αGpdhF (P < 0.01) allele frequencies in summers. Frequencies of these alleles were significantly positively correlated with environmental temperature, suggesting the adaptive significance of these allozyme polymorphisms. Frequency changes of the Odh locus (located on the third chromosome) showed no seasonal pattern and were not correlated with environmental temperature. Almost all short-term and long-term increases in AdhS frequency were accompanied by a corresponding decrease in αGpdhS frequency (r = –0.82, P < 0.001) and vice versa. Further analysis showed that gametic disequilibria between the Adh and αGpdh loci, which frequently occurred, were due to the presence of inversion In(2L)t located on the same chromosome arm and In(2L)t frequencies were positively correlated with environmental temperature. Gametic disequilibria between Adh and Odh and between Odh and αGpdh were hardly observed. Because In(2L)t is exclusively associated with the AdhS/αGpdhF allele combination, the observed correlated response in Adh/αGpdh allele frequencies is (at least partly) explained by hitchhiking effects with In(2L)t. This means that the adaptive value of the allozyme polymorphisms has been overestimated by ignoring In(2L)t polymorphism. Fluctuations in Adh allele frequencies are fully explained by selection on In(2L)t polymorphism, whereas we have shown that αGpdh frequency fluctuations are only partly explained by chromosomal hitchhiking, indicating the presence of selective differences among αGpdh genotypes in relation with temperature and independent of In(2L)t. Frequency fluctuations of αGpdh and In(2L)t are consistent with their latitudinal distributions, assuming that temperature is the main environmental factor varying with latitude that causes directly or indirectly these frequency distributions. However, the results of the tropical greenhouse population show no correlation of Adh (independent of In(2L)t) and Odh allele frequencies with environmental temperature, which may indicate that the latitudinal distribution in allele frequencies for these loci is not the result of selection on the F/S polymorphism in a direct way.
Many organisms show latitudinal variation for quantitative traits that is assumed to be due to climatic adaptation. These clines provide an opportunity to study the genetics of the adaptive process both at the phenotypic and the underlying molecular levels. Yet researchers rarely try to link variation in quantitative traits to their underlying molecular genetic basis. We describe a novel approach for exploring the genetic basis for clinal variation in size and stress traits in Drosophila melanogaster. We look for associations between genetic markers and traits that exhibit clinal patterns on the east coast of Australia using a single, geographically central population. There are strong associations between markers found within In(3R)Payne and variation in size, suggesting that this inversion explains much of the clinal variation in this trait. We also find that development time is associated with the Adh allozyme locus, cold resistance is negatively associated with the In(3L)Payne inversion and a genetic marker for Hsp70, a heat-shock protein, is associated with heat resistance. Finally we discuss the importance of inversions in clinal variation for quantitative traits and for identifying quantitative trait loci.
The four paracentric autosomal chromosome inversions In(2L)t, In(2R)NS, In(3L)P and In(3R)R are commonly polymorphic in natural populations of D. melanogaster in Australasia, North America and Asia, with latitudinal clines in the frequencies of each inversion in each region. In each region inversion frequency decreases with increasing distance from the equator, although the precise relationship between frequency and latitude varies between inversions and, for In(2L)t and In(2R)NS, among regions. Each inversion also shows a longitudinal cline in at least one region but none show such a cline in all three. Although no inversion's frequency is associated with the same climatic variable in all three regions, inversion frequencies are generally positively related to annual maximum temperature and, more particularly, minimum temperature and minimum rainfall. The directions of the latitudinal clines and the climatic associations are consonant with evidence from D. melanogaster that inversion frequencies decline in winter. They are also consonant with evidence from some other Drosophila species that inversion heterozygosities are lower at the geographic margins than at the centre of the species' ranges.