Download Modes of Selection and Recombination Response in Drosophila

ª 2004 The American Genetic Association
Journal of Heredity 2004:95(1):70–75
DOI: 10.1093/jhered/esh016
Modes of Selection and Recombination
Response in Drosophila melanogaster
C. F. RODELL, M. R. SCHIPPER,
AND
D. K. KEENAN
From the Department of Biology, College of St. Benedict/St. John’s University, Collegeville, MN 56321 (Rodell), Tuff Cut
Landscape, 115 Alabama St. SE, Lonsdale, MN 55046 (Schipper), and Department of Philosophy, Fairfield University,
Fairfield, CT (Keenan).
Address correspondence to Charles F. Rodell at the address above, or e-mail: [email protected].
A selection experiment for sternopleural bristle number in
Drosophila melanogaster was undertaken to analyze the
correlated effects on recombination. Replicate lines were
subjected to divergent directional selection and to stabilizing
selection. Recombination rates for markers on chromosomes
2 (dp-cn-bw) and 3 (se-ss-ro) were compared to those from
a control. All lines responded as predicted for bristle number.
Lines selected for both increased and decreased bristle
number exhibited significantly increased recombination rates.
The predicted recombination response from stabilizing
selection is suggested by our data, but only one comparison
is statistically significant. These results, taken with other
studies, support the proposal that genetic recombination
enhances individual fitness when populations are experiencing
environmental change. Less conclusively, our results suggest
that populations undergoing stabilizing selection may respond
by reducing their rates of crossing over.
Three types of data suggest that observed recombination rates
are the result of natural selection. First, genetic control for
both increased and decreased crossover rates between
nonsister chromatids has been demonstrated by selection in
laboratory populations of Drosophila melanogaster (Chinnici
1971; Kidwell 1972). Second, there is significant genetic
variation for genes influencing recombination rates in natural
populations of D. melanogaster (Brooks and Marks 1986).
Finally, recombination rates in D. melanogaster can change as
a correlated response to selection for other characters (Flexon
and Rodell 1982; Korol and Iliadi 1994; Sismanidis 1942;
Zhuchenko et al. 1985). These latter studies, which monitor
the correlation between recombination rates and the selected
character, illustrate that selection favoring individuals lying
near the extremes of a phenotypic distribution causes
a corresponding increase in the rate of recombination.
Apparently alleles that enhance rates of crossing over generate
more variation of the character under selection. Thus the
response to directional selection, regardless of the direction,
brings with it high recombination rate alleles. Conversely
then, if this is the case, alleles that lower recombination rates
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should produce a greater proportion of offspring near the
mean expression in the population. As a result, stabilizing
selection should decrease recombination rates. To our
knowledge, this response has not been demonstrated.
In this study we assess the recombination rate response to
both divergent directional selection and stabilizing selection
on a polygenic trait. The selected character is sternopleural
bristle number in D. melanogaster. Bristle number is influenced
by many genetic loci distributed throughout the genome (Jan
and Jan 1994), is highly heritable with largely additive genetic
variation (Mackay 1995), and lends itself to all modes of
selection. Quantitative effects on bristle number have been
attributed to regions of all three major chromosomes (X, 2, 3)
by both conventional Drosophila chromosome methods
(Shrimpton and Robertson 1988; Thoday and Boam 1959;
Thoday et al. 1964) and quantitative trait loci (QTL) mapping
(Gurganus et al. 1999; Lai et al. 1994; Lyman et al. 1999;
Nuzhdin et al. 1998). Likewise, all three major chromosomes
of D. melanogaster have genes that influence the recombination rate (Charlesworth and Charlesworth 1985). Thus D.
melanogaster provides a useful model organism with which to
test our predictions on recombination rate and the mode of
selection.
Materials and Methods
We established several isofemale lines from D. melanogaster
collected in central Minnesota (Stearns County). From
these, 10 inseminated females from each of 19 isofemale
lines were pooled to establish the initial source population.
All the selection lines were derived from this source
population.
Selected Lines
Selection was based on sternopleural bristle number. We
isolated 50 virgin females and 50 virgin males from the
source population, scored the bristle number, and selected
two pairs to initiate each selection line. We established three
types of selection lines with two replicates for each. The high
Brief Communications
lines (designated H1 and H2) were initiated from the four
flies of each sex with the highest bristle numbers, low lines
(L1 and L2) from the four males and four females with the
lowest bristle numbers, and the median lines (M1 and M2)
from four pairs of flies having a median bristle number of 18.
The high and low lines simulated directional selection and the
median lines represented stabilizing selection. Throughout
the experiment we maintained cultures at 25 6 18C. In
addition to the selection lines, we cultured a control line
under identical conditions except that each generation was
initiated with approximately 10 pairs of adults chosen at
random.
Selection
At approximately 2-week intervals, we isolated 20 virgin
females and 20 virgin males from each selection line. From
these flies we scored the bristle number and selected the
appropriate two pairs to parent the next generation. Selected
parents for H1 and H2 were those flies with the highest
bristle numbers, L1 and L2 the lowest bristle numbers, and
M1 and M2 those with 18 bristles, or as close to 18 as
possible. Selection continued for 25 generations except for
L2, which was lost after the 16th generation.
Recombination
We measured recombination rates on the second and third
chromosomes using stocks homozygous for the following
loosely linked recessive alleles: chromosome 2/dumpy (dp,
13.0) – cinnabar (cn, 57.5) – brown (bw, 104.5); chromosome
3/sepia (se, 26.0) – spineless (ss, 58.5) – rough (ro, 91.1). The
numbers are the standard map positions (Lindsley and
Grell 1968). At generations 15 and 25, we crossed 20 males
from each line individually to virgin females from each of the
marker stocks. We then backcrossed one F1 female from
each of these single-pair crosses to marker stock males
and scored the testcross offspring for recombinant phenotypes. The data are expressed as a recombination index,
representing the observed number of recombination events
divided by the total number of possible recombination
events. Because each chromosome has three markers, the
recombination index is computed by dividing the number of
recombination events among testcross offspring by twice the
total number of offspring, as it is possible to observe
a maximum of two events per individual. These results were
compared among selection lines and to the control
population.
Because we used loosely linked markers, we can assume
that multiple crossover events were common. Between any
two markers we score a single recombinant for an odd
number of crossovers, whereas an even number of crossovers
restores the parental arrangement. The sum of the odds will
be greater than the sum of the evens. While a higherresolution analysis would be possible had we employed more
markers with tighter linkage, our objective is simply to
compare relative recombination frequency between selected
lines and the control.
Results
Divergent Directional Selection
The results indicate that directional selection was successful
at both increasing and decreasing sternopleural bristle
numbers. The source population had a mean sternopleural
bristle number of 17.4 6 0.51 (mean 6 95% confidence
interval [CI]) and a range of 14 to 23. Each line selected for
increased bristle number exhibited a steady increase
throughout the 25 generations of selection, achieving mean
bristle numbers of 34.8 6 0.82 and 32.5 6 0.85 for H1 and
H2, respectively. Analysis of variance (ANOVA) indicates
that these values are significantly greater than the bristle
number of the source population (F2,127 ¼ 887.2; P , .0001).
Selection for low bristle number initially resulted in an
increase; for example, at generation 2, L1 had a mean of 19.6
6 0.54 and L2 had a mean number of 18.2 6 0.53. Bristle
numbers in L1 fell below the source population mean of 17.4
by generation 5 and continued to decrease to a mean value of
12.4 6 0.57 by generation 25, which is significantly less than
that of the source population (t88 ¼ 13.6; P , .0001). L2
numbers momentarily fell below the base population mean at
generation 5, but then bristle numbers were above this mean
for six of the next seven generations. By generation 13, L2’s
mean decreased to 16.2 6 0.53, and from this point it
decreased to a mean value of 14.5 6 0.53 at generation 16.
However, as early as generation 9, L2 was not as productive
as the other lines and it was lost after generation 16. At
generation 15, the means of L1 (13.2 6 0.64) and L2 (14.2 6
0.59) are significantly less than the mean bristle number of
the base population (F2,127 ¼ 55.8; P , .0001).
These response patterns are similar to those of other
bristle selection experiments (Barker and Cummins 1969;
Barnes and Kearsey 1970; Thoday 1958). This character
responds well to selection, and response to an increased
number of bristles is greater than is selection for a reduction
in number. An asymmetrical response is common and may
result from a number of different factors, including directional dominance and differential fitness between individuals
at the distribution extremes (Hedrick 2000). Barnes and
Kearsey (1970) did detect a dominance effect of approximately 0.45 in the direction of low bristle number when they
employed divergent directional selection. In this experiment,
L1 and L2 were generally less hardy than the other selection
lines, suggesting lower fitness among individuals expressing
fewer bristles in their phenotypes.
Stabilizing Selection
After 25 generations of selecting parents with 18 sternopleural bristles in our stabilizing selection lines, the means of M1
and M2 are 17.4 6 0.32 and 18.6 6 0.29, respectively.
Effective stabilizing selection is expected to decrease the
variation about the mean. Figure 1 illustrates the standard
deviation of bristle number each generation for populations
M1 and M2. For each population, the negative slope is
significantly less than zero, indicating effective stabilizing
selection.
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Journal of Heredity 2004:95(1)
Figure 1. The relationship between standard deviation of sternopleural bristle number as a result of stabilizing selection in
populations median 1 ( y ¼ 1.66 0.0225x; t24 ¼ 3.84, P , .001 for Ho:byx ¼ 0) and median 2 ( y ¼ 1.65 0.0267x ; t24 ¼ 7.81,
P , .001 for Ho:byx ¼ 0).
Recombination
Recombination indices for chromosomes 2 and 3 are
presented for the control and selected populations (generations 15 and 25) in Table 1. For each chromosome at each
generation tested, pooled heterogeneity G tests indicate
significant recombination index differences among populations. For each selected population, the recombination index
is compared to that of the control population by a 2 3 2
contingency test.
The most dramatic recombination responses are observed in H1 and H2, the lines that exhibited the greatest
response to bristle selection. H2 has a significant increase in
recombination frequency for chromosome 2 at both
generations 15 and 25, while H1 shows no significant change
in recombination activity for this chromosome. For chromosome 3, H1 has marked increases in its recombination
index at generations 15 and 25, and H2 shows a significant
increase at generation 15. At generation 25, H2 has an
elevated recombination index, which flirts with the conventional level of significance (v2 ¼ 3.70, df ¼ 1; P ¼ .054). These
results indicate that selection for increased bristle number,
a polygenic, morphological character, brought about a corresponding increase in recombination rates on chromosome 3
in both H1 an H2, and on chromosome 2 in H2.
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Recombination effects in the low lines are less pronounced. While L2, the poor-viability line, exhibited
a significant reduction in bristle number by generation 15,
it did not experience any change in its recombination index
compared to the control population (chromosome 2, P .
.70; chromosome 3, P . .80). At generation 15, L1 had
a significantly greater recombination index relative to the
control population for both chromosome 2 and 3. By generation 25, this comparison is not significant. The selective
response to bristle number corresponds to the recombination
index pattern. L1’s mean bristle number went from 17.4 6
0.51 at generation 0 to 13.2 6 0.64 by generation 15, to
12.4 6 0.57 at generation 25. While the bristle number difference between generations 0 and 15 is statistically significant, the difference between generations 15 and 25 is not
(t ¼ 1.80, df ¼ 78; P ¼ .075). It would appear that recombination increased as long as directional selection was effective,
but when the population could no longer respond to
selection for fewer bristles, there was a corresponding
reduction in recombination, reverting to a frequency indistinguishable from that of the control population.
The differences between replicates possibly result from
a founder effect. Each population was initiated with two pairs
(a total of eight genomes) drawn from the source population.
Brief Communications
Table 1.
Chromosome 2 and 3 recombination indices for selected populations (L1, L2, M1, M2, H1, H2) and the control
Chromosome
Generation
a
2
15
2
25b
3
15c
3
25d
Control
L1
L2
M1
M2
H1
H2
0.430
(1,016)
0.421
(688)
0.264
(712)
0.274
(975)
0.460*
(1,311)
0.436
(966)
0.295*
(1,224)
0.274
(1,089)
0.435
(1,050)
—
0.419
(847)
0.406
(922)
0.265
(1,026)
0.249
(980)
0.421
(921)
0.409
(1,035)
0.233*
(1,217)
0.258
(844)
0.431
(943)
0.441
(1,094)
0.304**
(943)
0.313**
(1,155)
0.471**
(1,128)
0.456*
(1,201)
0.297*
(1,040)
0.300
(1,308)
0.261
(1,165)
—
Numbers in parentheses represent the number of testcross offspring scored.
* Significantly different from control at P , .05 (2 3 2 contingency chi-square); ** P , .01.
a
Pooled heterogeneity G test, GH ¼ 10.86, P , .05.
b
Pooled GH ¼ 15.38, P , .01.
Pooled GH ¼ 30.56, P , .001.
c
d
Pooled GH ¼ 30.12, P , .001.
As a result, H1 and H2 exhibited similar recombination
responses for chromosome 3, but not for chromosome 2. L2
did not do nearly as well as L1 in either selection response or
recombination activity.
Our working hypothesis predicted that the recombination index would decrease as a result of stabilizing selection.
While only one comparison (M2, chromosome 3, generation
15) is statistically significantly different from the control,
seven of the eight comparisons of M1 and M2 to the control
have a lower recombination index than the control value.
This distribution, seven of eight, has a probability equal to
0.03 if values less than or greater than the control are equally
likely. These results suggest a reduction in recombination
activity as a result of stabilizing selection on bristle number,
but they are less conclusive than the results for directional
selection. Stabilizing selection’s less dramatic response
compared to directional selection may reflect the fact that
natural selection acts on sternopleural bristle number in
a stabilizing manner (Barnes 1968; Mackay 1995; Simpson et
al. 1999; Thoday 1958). Hence the recombination rate
influences on this character have been selected naturally for
lower rates and, as a result, there may be less potential for
reduced recombination rates than for enhanced rates.
For those comparisons where the recombination response is significantly different from that of the control, it is
worth noting the chromosome location. Chromosome 2 in
the source population had a recombination frequency of
0.386 between markers dp-cn, and 0.443 between cn-bw, that
is, 46.6% of the observed recombinant events occurred
between the first two markers and 53.4% between the
second two. Likewise for chromosome 3, the source population has a recombination frequency of 0.274 (50.4%)
between se-ss, and a frequency of 0.270 (49.6%) between ss-ro.
Among selected populations, chromosome 2 changes
occurred most significantly between cn-bw, with this region
comprising 56.2%, 58.1%, and 57.0% of the total recombinant events for L1 generation 15, H2 generation 15, and H2
generation 25, respectively. Within chromosome 3, the
region between se-ss displays the greatest response in all
cases. Recombination responses in this region increase to
52.0% (L1), 54.1% (H1), and 53.2% (H2) in generation 15,
and 55.3% (H1) in generation 25. Population M2 shows
a marked decrease in this same region, with recombination
events accounting for 47.7% of the total. These results are
consistent with the positions of major sternopleural bristle
loci identified by mapping (e.g., Nuzhdin et al. 1998;
Shrimpton and Robertson 1988).
Discussion
The present study has two objectives. First is to test whether
the response to divergent directional selection, both increased and decreased expression of a polygenic character,
will alter recombination frequency among the offspring of
favored individuals. Evolutionary theory postulates that
populations must be genetically variable in order to evolve.
With directional selection, the capacity of a population to
respond is in large part dependent on its ability to release its
latent variability and expose it to selective action. The most
immediate source of genetic variation is that generated by the
process of recombination. Individuals with the highest rates
of recombination should, on average, produce genetically
more variable offspring. When selection favors the population extremes, favored individuals are more likely to have
descended from high recombination-rate parents. This result
has been demonstrated by selection in one direction for
increased scutellar bristle number (Sismanidis 1942), increased sternopleural bristle number (Thoday et al. 1964),
and increased DDT resistance (Flexon and Rodell 1982); for
divergent directional selection on geotaxis (Korol and Iliadi
1994); and for temperature fluctuations (Zhuchenko et al.
1985). The present study further confirms these results by
employing selection for both increased and decreased
sternopleural bristle numbers.
The results from divergent directional selection show
that increased recombination does not require gametic
disequilibrium between genes affecting recombination rate
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Journal of Heredity 2004:95(1)
and genes influencing the selected character in order for high
recombination-rate alleles to increase in frequency (Felsenstein 1965; Hedrick 1982). Rather, these data, along with the
other divergent directional selection study (Korol and Iliadi
1994), argue that high rates of recombination produce
a disproportionately greater proportion of individuals at the
population extremes, and the recombination response is not
due simply to hitchhiking.
Our second objective tests whether stabilizing selection
results in a corresponding decrease in recombination rate.
Given the above discussion, it follows that individuals with
lower recombination rates should produce less variable
offspring. Mather (1943) suggested that selection for an
intermediate optimum will cause gametic disequilibrium in
such a way as to reduce the amount of genetic variation, that
is, reduce recombination. It follows that mean fitness in
a constant environment will be greatest when recombination
is absent (Charlesworth 1993). Stabilizing selection should
select a disproportionately greater number of individuals
whose parents have low recombination rates. Our results
show a general decline in recombination activity resulting
from stabilizing selection, but just one of the eight comparative tests proved statistically significant.
It is generally agreed that understanding the evolutionary
cause of recombination is key to explaining the prevalence of
sexual reproduction (Bell 1982; Maynard Smith 1978;
Williams 1975). A recent experiment employing D. melanogaster compares the fate of beneficial mutants in sexual and
asexual populations (Rice and Chippendale 2001). Their
results support the explanation that recombination is
advantageous because it allows populations to adapt more
rapidly by accumulating beneficial mutants and by reducing
the accumulation of harmful mutants. The results reported
here add to those studies supporting the general conclusion
that recombination persists to enhance individual fitness in
response to changing environmental conditions. In contrast,
an analysis of second chromosomes from collections of D.
melanogaster indicates a negative correlation between recombination frequency and fitness (Tucic et al. 1981). This
latter study differs from those previously mentioned in that
the subjects were not subjected to further selection pressure.
While many studies addressing this question utilize D.
melanogaster, data from other organisms add relevance. For
example, higher chiasma frequencies are observed when
selecting for increased body size in mice (Gorlov et al. 1992).
With yeast, increased sporulation rates are found in
populations subjected to highly variable environments (Wolf
et al. 1987). A survey of chiasma frequencies among 21
mammalian species suggests that recombination is necessary
to keep pace with changing biotic relationships (Burt and Bell
1987). As in D. melanogaster, these studies support the contention that recombination rate is positively correlated to individual fitness when populations are subjected to selection.
The extent, then, to which Mendelian populations
respond to changing environmental conditions influences
the rates of genetic recombination through crossing over.
Recent studies support the interpretation that selection is
a common force shaping patterns of variability in natural
74
populations of Drosophila (Andolfatto and Przeworski 2000,
2001). Further, it appears as though biotic factors are of
prime selective importance (Fay et al. 2002). Biotic
interactions, coevolutionary forces, are likely to be persistent
and directional, maintaining an advantage to recombination
(Levin 1975). Additional studies on a wider range of
organisms and on stabilizing selection’s influence on crossing
over should further enhance our understanding of genetic
recombination and evolution.
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Received April 2, 2003
Accepted September 1, 2003
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Corresponding Editor: Rob DeSalle
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