Biological Journal o f t h e Linnaan SocieQ (1988), 35: 49-68. With 4 figures
Evolutionary rates: effects of stress
upon recombination
P. A. PARSONS
Department of Genetics and Human Variation,
L a Trobe University, Bundoora, Victoria, Australia, 3083
Received I4 May 1987, accepted for publication 29 March 1988
There is increasing evidence that ecological variables involving stress are important in determining
evolutionary rates. This paper incorporates recombination into this scenario.
I n Drosophila melanogaster, recombination increases at developmental temperatures above and
below normal culture temperatures, giving a U-shaped curve which is most pronounced in
centromeric regions; however, at near lethal temperature extremes there is some evidence for a fall
in recombination. More limited data from other organisms are generally consistent with this
conclusion. Nutritional stress in the form of starvation increases recornbination in D. melanogaster,
and behavioural stress has been found to increase recombination in male mice.
In natural populations recombination is under complex genetic control analogous to other
quantitative traits. In D.melanogaster in a novel environment, there is evidence that additive genetic
variability for recombination is higher than in a standard laboratory environment. During selection
in populations exposed to extreme stress increased recombination may occur; this implies that in
marginal (stressful) habitats, variability generated by recombination may increase.
In D. melanogaster, structural heterozygosity due to inversions in one part of the genome tends to
increase recombination in the remainder of the genome in a qualitatively similar manner to, and
cumulative with, direct environmental effects especially temperature. Substantial recornbination
should he inducible under combinations of karyotypes and environments deviating from existing
circumstances, especially if the suggestion that effects are often synergistic due to a dependence
upon available energy levels can be confirmed.
KEY WORDS:-Evolution - recombination - Drosophila mice
stress - chiasmata - genomic stress - interchromosomal effects.
~
~
temperature stress - nutritional
CONTENTS
Introduction . . . . . . . . . . .
Drosophila . . , . . , . , . . , .
Temperature . . . . . . . . . .
Nutrition . . . . . . . . . . .
Age . . . . . . . . . . . .
Other organisms . . . . . . . . . .
Temperature . . . . . . . . . .
Age . . . . . . . . . . . .
Behavioural stress
. . . . . . . .
Genetic variation in recombination
. . . . .
Recombination and adaptation
. . . . . .
Genomic and environmental stresses: are they cumulative?
. . . . . . . . .
Acknowlcdgrments
References
. . . . . . . . . . .
0024-4066/88/090049
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0 1988 The Linnean Society of London
50
P. A. PARSONS
INTRODUCTION
One approach to an understanding of evolutionary rates comes via a fusion of
ecology and genetics when the climate and hence the physical environment is
stressful (Parsons, 1986). The stresses tend to be of such severity that continuous
exposure is rapidly lethal. These are conditions exemplified by short bursts of
extreme stress occurring at climatic and ecological margins where just a small
environmental perturbation could lead to lethality. A major difficulty in the
definitive study of evolutionary rates under environmental stress therefore
resides in selecting the elusive stress where fertile survivors occur, yet lethality is
close. Experiments at this critical boundary pose logistic difficulties not apparent
in most studies in experimental evolutionary biology where more optimal
environments are chosen. Ideally, a range of stresses in a well-designed
experiment is needed to detect the critical boundary, which must vary among
species and populations according to previous selection regimes.
The evidence for this boundary derives from a variety of sources including:
( 1 ) The biogeographical significance of extremes of cold and heat in
predicting the distribution of Australian floral types and Drusuphila species,
together with laboratory experiments on the resistance of Drusophila to extreme
stresses (Nix, 1981; Parsons, 1983).
(2) The importance of extreme climatic events in predicting limits to
agricultural viability of certain crop plants in northern Europe (Parry, 1978).
(3) Associations between extreme stresses and certain genotypes in natural
populations of Drosophila, D a m and Avena (Clegg & Afiard, 1972; Parsons,
1980).
(4) The observations of major morphological changes in natural populations
under conditions of such severe climatic stress that most of the population is
decimated, as in the Galapagos finch Geuspirafurtis (Boag & Grant, 1981).
(5) The development of heat shock proteins at temperatures that on
continuous exposure would be lethal (Atkinson & Walden, 1985; Lindquist,
1986).
(6) The importance of adaptive responses of enzymes to temperature stresses,
especially in fish and higher plants (Somero, 1978; Simon, 1979; Simon, Charest
& Peloquin, 1986).
There is a consistency across integration levels from the biogeographic to the
molecular, involving stresses close to the threshold where continuous exposure
would wipe out populations. Under these conditions, phenotypic and genotypic
variability tends to be high, especially for quantitative traits important in
determining survival (Parsons, 1986).
The number of species available for recombination studies is very restricted,
and Drosophila melanogaster experiments predominate. Following Andrewartha &
Birch (1954), the distribution and abundance of each species is determined by
combinations of the physical and biotic factors that are required for survival and
reproduction of its individuals. Considering Drosophila, the broad species
distributions can be explained by tolerances to extreme temperatures within the
melanugaster subgroup and across the genus (Stanley, Parsons, Spence & Weber,
1980; Parsons, 1983). It is therefore important to consider recombination under
temperature extremes. Considering resources, those Drosophila species that do
RECOMBINATION UNDER STRESS
51
not utilize fermented fruits d o not have the biochemical phenotype for major
range expansions as shown by ethanol utilization studies (Holmes, Moxon &
Parsons, 1980). Hence recombination under variable levels of ethanol and
related metabolites should be considered. I n the wild, nutrition is expected to be
less adequate than under laboratory conditions (Boulttreau, 1973) emphasizing a
need to consider recombination under varying nutritional levels. I n all cases,
environments which are plausible in nature will be emphasized. An ever
increasing literature on recombination affected by exotic chemicals will
therefore not be considered. In other words, the object is to examine stresses of
perceived evolutionary significance based upon the habitats and resources
utilized by various species.
Based upon the general conclusion that phenotypic and genotypic variability
is highest under conditions of environmental stress, the hypothesis is that
recombination is lowest under optimal conditions, so that recombination
increases as the environment becomes progressively more stressful. For
temperature, this means that extremes of both cold and heat should increase
recombination giving a U-shaped curve. More generally, any shift from the
environment to which organisms have become adapted should increase
recombination.
DROSOPHILA
Temperature
Within the first decade of genetical experiments on D.melanogaster, Plough
(1917, 1921) found that recombination especially in centromeric regions of
chromosomes 2 and 3 increased when the temperature at which the female fly
developed was increased or decreased from 25°C) the normal laboratory culture
temperature. For the black-purple region which is just proximal to the
centromere in chromosome 2, Plough (1917) found threefold increases in
recombination at 13 and 3 1°C (Fig. 1). Qualitatively similar results were
obtained by Graubard (1932) over the narrower range of 14-30°C with a
twofold increase in recombination at the extremes. Minor temperature
Olr
9
I
13
I
I
17.5
22
I
I
I I
27 29 313;
Temperature ( " C )
Figure 1. Weighted values for the black-purple region of chromosome 2 of Drosophila rnelanogaster
plotted to show the e f k t of temperature on crossing over (after Plough, 1917).
P. A. PARSONS
52
fluctuations at stressful extremes can therefore have major effects upon
recombination. Plough (1921) did not find a temperature effect for the X
chromosome, but Stern (1926) found increased recombination at 30"C, in
comparison with 25"C, in the Bar-boobed region, a segment adjacent to the
centromere. Later experiments include those of Hayman & Parsons (1960) who
found more recombination close to the centromere at 30°C compared with
20"C, and Chandley (1868) who found that crossing over increased in the
proximal region adjacent to the centromere and decreased at the distal end
following a brief high temperature treatment at 34°C.
These results suggest that stress increases recombination especially in
centromeric regions. The stress interpretation is given weight because, at 30"C,
Hayman & Parson (1960) found irregular variations in recombination
presumably due to developmental instability. Furthermore, coincidence values
were higher at 30 than at 20"C, suggesting less genetical interference under
stress and hence more recombination. A re-analysis of Graubard's (1932)
chromosome 2 data by Hayman & Parsons (1960) also indicates less interference
in the cold at 14.0 and 16.5"C and in the heat at 30°C (Table 1).
Interestingly, this effect occurs in a distal chromosome segment al-tx-6 where
recombination fractions are little affected by environmental extremes in
comparison with tx-6-pr which is adjacent to the centromere, so that coincidence
and recombination frequencies may show some independence from each other
(Rendel, 1957). Thus, in this example, one effect of stressful temperatures is to
alter the pattern of recombination by increasing the proportion of double
recombinants even where the number of single recombinants is little affected.
In the field, it is difficult to collect D.melanogaster below about 12°C in winter
in temperate zone habitats. At around 12"C, flying activity is minimal and flies
tend to walk sluggishly over piles of rotting fruit, indicating that this
temperature is on the threshold where species continuity is under threat because
mating, oviposition and flying are highly restricted (Parsons, 1977, 1983). Both
mating and oviposition increase linearly with temperature between 12°C and
20°C (McKenzie, 1975), and data are needed to cover the upper threshold in
the range 30-31°C. Plough's (1917) data give a weighted recombination value
for the b-pr segment of 8.7% at 29°C and 18.2% at 31"C, compared with a
control value of 6.0y0, which indicates the sensitivity of recombination to minor
temperature changes under stressful conditions. Both at low and high
temperatures, therefore, there is a sharp escalation of recombination close to
environmental conditions where species continuity is threatened in nature.
For females grown at 25"C, the sensitive period for enhancing recombination
is restricted to days six and seven or 120-168 h following oviposition, in
TABLE
1. Recombination and interference in chromosomes 2 of Drosophila melanogaster calculated
by Hayman & Parsons (1960) from data of Graubard (1932)
Tempcrature ("C)
at which data
were collected
14
16.5
25
30
Recombination in segment:
Coincidence
a!-tx
tx- b
b-pr
al-tx-b
tx-b-pr
9.83k0.50
10.82+0.41
10.92f0.43
11.85f0.48
30.82f0.78
32.15k0.52
27.01 f0.61
28.87f0.67
13.17f0.57
10.39+0.40
5.85 f0.32
9.92f0.45
0.273k0.048
0.321 k0.037
0.218f0.036
0.440f0.048
0.507&0.053
0.423+0.041
0.228 f 0.050
0.541 k0.058
RECOMBINATION UNDER STRESS
53
TABLE
2 . Heat effect on crossing over and coincidence in the five major chromosome arms of
Drosophila melanogaster (after Grell, 1978a)
Crossing over in regions:
1
2
3
Coincidence in adjacent regions
Total
1,2
2,3
3,4
4,5
car-y*
5.5
10.5
68.5
82.4
0.16
0.80
0.71
0.83
0.24
0.51
0
0.26
j-Bl
9.2
16.6
54.2
67.7
0.03
0.19
0.13
0.27
0.28
0.23
0.94
0.75
Pu-sp
12.1
14.9
49.7
71.9
0
0.24
0.29
0.34
0.19
0.48
0.12
0.49
4
5
f-car
7.5
9.5
hi
sc-cu
cu-u
U-f
X
25°C
35OC*
11.1
15.1
21.3
22.1
23.1
25.2
2L
25°C
35'C*
al-shu
5.1
6.9
shu-cl
14.1
13.1
cl-fr
10.2
12.2
R
25°C
35"C*
stw-cn
1.6
8.9
cn-sea
11.0
16.9
3L
25°C
35"C*
ue-Coa
7.1
11.0
Coa-h
15.4
21.5
h-th
21.8
32.0
th-p
6.8
28.1
51.1
92.6
0.17
0.85
0.28
0.74
0.33
1.00
st-sbd
25°C
35OC*
sbd-8
18.8
23.8
2-TO
3R
ro-ca
12.3
18.5
82.0
114.8
0.54
0.60
0.64
0.39
0.18
0.33
25.8
41.9
15.6
18.8
sca-nwD nwD-Pu
12.3
12.7
14.0
17.2
24.9
30.6
*35OC for 12 h at varying ages between 126 and 156 h for different chromosome arms.
particular the period between pupation at 132-162 h which corresponds closely
to the time of DNA replication and synapsis of the S-phase during premeiotic
interphase (Grell, 1973, 1978a, 1984; Grell & Day, 1974). The periods of peak
response using heat treatments consisting of temperature pulses of 12 h at 35°C
varied between arms: 2L (126-138 h), X (132-144 h), 3L and 3R (138-150 h
and 2R (144-156 h). Heat effects on crossing over and coincidence in the five
chromosomes arms are summarized in Table 2 from data in Grell (1978a)
indicating substantial increases in recombination especially in proximal regions.
In the distal regions increases are of lesser magnitude in the four autosomal arms
than the proximal regions, and there is approximately equal enhancement at
both ends of the X chromosome. I n addition, genetical interference tends to be
lower at 35°C. Periods of extreme temperature stress can therefore have
substantial effects upon recombination at critical times. In addition, Grell
( 1978a, b) considered recombination in a small heterochromatic region, It-stu,
spanning the centromere of chromosome 2. Following exposure to 35°C for 12 h
in the 150-162 h period, the recombination percentage increased by 3600%
from 0.00047 to 0.01694. For region BI-lt to the immediate left of the
centromere the recombination percentage increased by 3200% from 0.042 to
1.34 in the 156-168-h period (Grell, 1978a, b). The effects upon recombination
can therefore be dramatic when applied a t critical developmental stages in
certain regions of the genome.
I n summary, especially in centromeric regions recombination increases and
interference decreases at temperatures above and below normal culture
temperatures, giving a U-shaped curve.
Nutrition
Boulktreau's ( 1978) observations on ovarian activity and reproductive
potential in a natural population of D. melanogaster suggest the occurrence of
54
P A PARSONS
long periods of nutritional stress in nature whereby flies only rarely have the
opportunity to utilize their genetic reproductive level. Hence nutritional stress
could have substantial evolutionary consequences as has been demonstrated in
the Galapagos finch, G. fortis (Boag & Grant, 1981), following a major drought.
The effect of availability of food during the larval stage upon recombination in
D.melanogaster was studied by Neel (1941) who grew larvae at 26°C and
separated them into two groups at 70 h of age; the control group completed
development under normal nutritional conditions, while larvae belonging to the
other group were placed in vials with nothing but absorbent tissue moistened
with water. The direct effect of starvation stress was shown by the mean weights
of newly eclosed female flies: 1.11 mg from the control larvae and 0.64 mg from
the partially starved larvae. Based upon five widely separated loci on
chromosome 3, h-th-cu-sr-e‘, Neel ( 1941) found that recombination was increased
along the whole region by 0-15y0 in the starved group (Fig. 2). This contrasts
with the much larger temperature effects which tend to be localized to
centromeric regions. There is a need to study recombination for all
chromosomes under severe nutritional stress. Even so, the tendency towards
increased crossing over under adverse conditions would lead to a larger number
of new factor combinations under just those conditions when novel phenotypes
may be favoured.
Species such as D. melanogaster are attracted to fermented fruit baits and
utilize ethanol as a resource. Under laboratory conditions there is substantial
variation in concentrations of ethanol (in vapour form) utilized as a resource
both within and among species which bears some relationship with habitat
(Parsons, 1983). Kilias, Alahiotis & Onoufriou (1979) found a n increase in
recombination in chromosome 3 of 10-15~0 in a Swedish C wild stock
homozygous for the alcohol dehydrogenase Adh” allele when either 20/,ethanol
or 2% propanol was added to the food medium. Ethanol at this concentration
cannot be regarded as stressful since it enhances longevity (Parsons, 1983), and
indeed there was no detectable effect on recombination in a Canton-S stock
homozygous for the AdhS allele.
This result leads to a number of experimental possibilities. With ethanol in
the food medium, longevity is reduced at concentrations above 6% in flies from
temperate-zone habitats (McKenzie & Parsons, 1972). Hence, recombination
experiments over a range of ethanol concentrations are needed. Considering
exposure of adults to ethanol vapour, there is a threshold between ethanol used
as a resource (i.e. longevity is increased) and a stress (i.e. longevity is reduced)
at concentrations ranging from 6% in tropical populations to more than 12% in
temperate-zone populations so providing a wide range of possibilities for testing
(Parsons, 1983). In addition, there are quantitative differences involving ADH
enzyme levels in different genotypes such as between Adh’Adh” us. AdhSAdhSand
Ziolo & Parsons (1982) found that the longevity of Adh’Adh” was less than that
of AdhSAdhSunder a range of ethanol vapour concentrations, so that the effect of
ethanol upon recombination should be greater in the former than the latter
genotype which is consistent with Kilias et al. (1979).
Ethanol is metabolized to acetic acid via acetaldehyde. A major contrast
between ethanol and acetic acid as metabolites is apparent from studies on an
Adh-null (Adh“‘) mutant where concentrations above 0.50/, ethanol are stressful
for adults (Parsons & Spence, 1981a), while the utilization of acetic acid is close
RECOMBINATION UNDER STRESS
.\
55
----- Control flies
0
-Experimental flies
4
30
2
6
10
14
16
22
26
Days after eclosion
Figure 2. A comparison of control Drosophila melanugaster with those developing from partially
starved larvae, incorporating the relation between age for recombination in the third chromosome
(after Neel, 1941).
to wild strains. I n the presence of ethanol, it could be argued that A h n z mutants
are in a state of metabolic stress by comparison with wild type strains, and so
effects upon recombination should be greater for a given stress-assessed in
terms of effects upon longevity-than in wild types. I n this case therefore, the
genotype is central in determining the level of environmental stress.
Finally, experimental possibilities are available for the intermediate
metabolite acetaldehyde. Even though it can be highly toxic, low concentrations
must occur in nature; it is used as a resource at low concentrations by some
Drosophila species (Parsons & Spence, 1981b) . Experiments on other compounds
(especially methanol, isopropanol, n-propanol and propionic acid) that are
common in Drosophila food would be of interest, and many have been shown to
be utilized as resources by Drosophila (Van Herrewege, David & Grantham,
1980; McKechnie & Morgan, 1982; Hoffmann & Parsons, 1984). Perusal of
general articles on the nutritional requirements and the biochemistry of growth
in Drosophila would undoubtedly reveal other experimental possibilities (see, for
example, Sang, 1978; Robertson, 1978) bearing plausible relationships with
habitats in nature.
Age
I n his larval starvation experiments, Neel ( 1941) studied recombination over
a range of ages from the time the female eclosed (Fig. 2), and found an initial
high in crossing over followed by a sustained low. Neel then reviewed the
situation more generally and noted that in seven studies involving chromosome
3 there was an initial high in the frequency of crossing over followed by a
decline in all cases except one. Some investigators argue for an initial decline
followed by a second, less pronounced, high and then a second decline,
suggesting periodic fluctuations in the amount of recombination; however, the
statistical significance of these fluctuations is difficult to assess. I n a study of the
entire third chromosome Bridges (1927) found that the region st-jf, which
contains the centromere, showed the largest decrease from the initial high,
regions pp-ss and D-st adjacent to and on either side of the centromere show
56
P. A. PARSONS
comparably large decreases, and those at the end of the chromosome the least
effect. Age effects have also been found for the X chromosome (Stern, 1926;
Hayman & Parsons, 1960), and for the second chromosome (Plough, 1917,
1921), all showing initial high values.
While the magnitude of age effects may be quite substantial in centromeric
regions temperature effects appear greater, but critical comparative experiments
are needed in the vicinity of the centromere.
OTHER ORGANISMS
Temperature
Temperature effects upon recombination have been studied in a number of
other eukaryotic organisms including the nematode Caenorhabditis and the fungi
Neurospora, Sordaria, Coprinus and Schizophyllum.
In Caenorhabditis elegans, Rose & Baillie (1979) found that recombination
increased three-fold between a pair of closely linked markers as temperature
increased from 13.5 to 26.0"C (Fig. 3). In Neurospora crassa, Rifaat (1959) found
a positive correlation with temperature over the range 17-3O0C, while Towe &
Stadler (1964) found a minimum a t 25°C and a maximum at 18°C. McNellyIngle, Lamb & Frost ( 1966) examined the relationship between temperature
and recombination in several crosses over the entire range (15-30°C) at which
the sexual cycle can be completed. A minimum was found at the temperature at
which N . crassa is normally incubated (25"C), and recombination consistently
increased towards higher values as temperatures deviated from 25°C. This
parallels Plough's (1917) data in D.melanogaster, and emphasizes the need for
studies to cover the entire temperature range for fertile offspring. I n Sordaria
brevicolis, temperature treatments well before meiosis gave a U-curve
relationship, while in S. jmicola a linear increase in recombination occurred with
increasing temperature (Lamb, 1969). I n Coprinus lagopus, Lu ( 1969, 1974)
found that pulses of both high (35°C) and low (5°C) temperatures increased
genetic recombination. Cold treatment appears more effective than heat
treatment, since the maximum recombination was increased 220% by cold and
95% by heat treatment. In Shizophyllum commune attempts to generalize the
specific effects of temperature failed, since Stamberg & Simchen (1970) found
that recombination within one mating factor, A, was constant and low between
15°C and 30°C then increased abruptly between 30" and 32"C, while within the
mating factor B the effect of temperature was largely reversed. More generally,
following a consideration of additional adjacent and non-adjacent chromosomal
regions, they concluded that a temperature change need not affect
recombination frequencies throughout the genome, and that the effect of
temperature in any particular region can vary from cross to cross. Hence the
effect of temperature is both region-specific and genotype-specific implying a
degree of fine control of recombination.
Summarizing, these selected examples offer suggestive evidence for higher
recombination at temperature extremes. Generalizations are difficult since
comprehensive experiments covering the entire temperature range over which
fertile offspring can normally be produced are needed. Even then, it may be
difficult to generalize because of varying results according to genotype and
chromosome region.
RECOMBINATION UNDER STRESS
I0
14
18
Temperature
22
57
26
("C)
Figure 3. The effect of temperature on the frequency of recombination between dpy-5 and unc-15 in
Caenorhabdztir elegans (after Rose & Baillie, 1979).
Age
Experiments in tomatoes with two seedling mutants (a, arthocyaninless; hl,
hairless) showed a significant decrease in crossing over associated with ageing
(Griffing & Langridge, 1963). Large quantities of data were readily obtainable
since the four phenotypic classes derived from two seedling mutants can be
classified within 3 weeks of placing seeds on moistened filter paper. A fall in
recombination with maternal age has been found in the mouse, Mus musculus, for
data for chromosomes V and XI11 (Fisher, 1949; Bodmer, 1961; Reid &
Parsons, 1963). Considering male heterozygotes, however, the data were
inadequate, showed no trends, or tended to show a slight increase in
recombination with paternal age (Wallace, 1957; Reid & Parsons, 1963). Not
all mammalian data show trends as described, for example in an extensive
analysis of horse data, no evidence of an age effect was found (Anderson &
Sandberg, 1984). However, even though data may be extensive, they could be
inadequate at extreme ages. I t is not therefore surprising that in human data,
age-related changes in chiasma frequencies and recombination have been found
in some cases but not in others (Weitkamp et al., 1973; Elston, Lange &
Namboodiri, 1976). Compared with experimental organisms such as the mouse,
however, it is difficult to obtain data to cover age extremes.
Summarizing the above and earlier comments there is some evidence for a fall
in recombination with maternal age in a wide range of organisms, but there is
no evidence for a corresponding paternal age effect. The maternal environment
of the primary oocytes changes substantially with age and such developmental
changes may have metabolic effects which affect the developing eggs and hence
the recombination process. Since meiosis occurs later in males than in females, a
differing effect of age in males compared with females is not surprising.
Behauioural stress
Belyaev & Borodin (1982) studied crossing over between the Ra and a loci of
chromosome V in Mus musculus, by crossing R a + / a + males with a + / a + females. A
control group of males was kept under normal conditions. Mature 2-month-old
males were subjected to stress consisting of placing 30 males in cages
58
P. A. PARSONS
50 x 30 x 15 cm which resulted in extremely aggressive collisions for a period of
10 days beginning 21 days before mating. This led to a stress reaction which was
manifested by a substantial increase in additive genetic variation for preimplantation mortality, litter size, relative adrenal weight and relative thymus
weight by comparison with the control population. From the dynamics of
spermatogenesis in mice, Belyaev & Borodin (1982) concluded that the females
in the above cross were inseminated by spermatozoa at meiosis during stress. I n
the control group of males, the recombination percentage was 23.95 & 1.29,
while in the stress-treated males it was 31.03+2.11, so that stress causes an
increase in the frequency of crossing over.
GENEIIC VARIKI'ION IN RECOMBINATION
It is important to place environmental effects into the context of genetic
variation for recombination in natural populations. Lawrence ( 1963) crossed
five inbred strains of D. melanogaster in all combinations and the frequency of
recombination between eight marker genes on a common pair of
X chromosomes was scored among the backcross progenies of the parental lines
and their 20 Fl's. T h e results indicate that recombination is controlled
polygenically and that the additive component of variation is paramount, since
there was only slight dominance and no genic interaction. The experiments
were carried out at 25"C, the standard laboratory environment, and 18"C, a
novel environment. O n analysing the data separately at the two temperatures, it
turned out that significant additive genetic variation at 25°C was restricted to
the two distal segments of seven considered, whereas at 18°C additive genetic
variation involved all segments. This result is consistent with the general
phenomenon of high genetic variability under novel conditions, including the
adaptation of organisms to laboratory conditions (Parsons, 1986; Kohane &
Parsons, 1986), so that the interaction of genotype and environment in the
determination of recombination can be quite complex.
Brooks & Marks (1986) took six lines based upon second chromosomes
extracted from a natural population, and studied recombination using multiply
marked second, X and third chromosomes. Recombination in the second
chromosome varied in both amount and distribution. The second chromosomes
were associated with variation in both the amount and distribution of crossing
over in the X chromosome, and in the amount but not the distribution of
crossing over in the third chromosome. The total amount of crossing over on a
chromosomal basis varied by 12-14%. At the regional level, the range was
16--38y0, although one small region varied two-fold. Lines with less crossing
over in one chromosome generally had less in others, indicating that modifiers of
recombination can affect more than one chromosome.
These and other papers (e.g. Levine & Levine, 1955; Green, 1959; Clegg,
Horch & Kidwell, 1979) indicate varying recombination rates among stocks of
D. melanagaster and D. pseudaobscura. These results, together with the high
additive component found by Lawrence (1963), indicate that selection for
recombination should normally be successful as has been found (e.g. Detlefson
& Roberts, 1921; Parsons, 1958; Allard, 1963; and more recently Chinnici,
1971; Kidwell, 1972; Charlesworth & Charlesworth, 1985). The order of
magnitude of the change in such quantitative experiments rarely involved more
RECOMBINATION UNDER STRESS
59
than a doubling or halving of recombination, which is a far smaller effect than
some of the environmental effects discussed, in particular temperature. Even so,
attempts at localizing genetic activity for recombination have been successful;
for example, following selection for increased recombination in D. melanogaster,
Charlesworth & Charlesworth ( 1985) found recombination modifying genes on
the three major chromosomes. Mapping experiments revealed at least four genes
concerned with the difference between the high selected line and the control line
interacting in a complex fashion. They conclude that the genetic control of
recombination is exceedingly complex, and that they only managed to obtain a
partial picture of the range of genetic control. Studies at this level are therefore
consistent with a conventional quantitative trait adjusted to an optimum.
Additional to variation of a quantitative nature are mutants of major effect.
For example, Sandler, Lindsley, Nicoletti & Trippa (1968) constructed
homozygotes from nature of chromosomes 2 and 3 of D. melanogaster, and
studied crossing over in the X and segregation in the X and in chromosome 4
for the purpose of discovering meiotic mutants in chromosomes in nature, i.e.
mutations affecting one or more of the meiotic processes. A number of specific
mutants were found. A comparison of the variance in X chromosome
recombination among females carrying the various autosomal sets from natural
populations revealed that a significant fraction of the total variance in crossing
over was attributable to genetic differences among the autosomal sets from
nature, indicating the presence of many meiotic mutants in nature.
Recombination has been studied extensively in viruses, yeasts and fungi
(Catcheside, 1977) but mostly to understand mechanisms rather than variation
from an evolutionary viewpoint. However, Catcheside ( 1975) has recorded
polymorphism for recombination genes at three different loci in commonly used
laboratory stocks of Neurospora crassa. These loci control levels of recombination
in a number of different regions scattered in three different chromosomes so that
differing recombination rates under genetic control are a feature of any
organism where there are appropriate studies.
RECOMBINATION AND ADAPTATION
Arguments presented here and elsewhere (Mayr, 1963) indicate a dynamic
equilibrium between factors increasing and decreasing variability in
heterogeneous and homogeneous environments respectively. Hence, in a
homogeneous environment when a population is tending towards an
equilibrium, a tightening of linkage between interacting fitness loci would be
expected (Fisher, 1930) although this process does not go to the ultimate limit of
zero (Turner, 1967). Conversely, a loosening of linkage would be the
expectation in varying environments (Charlesworth, 1976; Maynard Smith,
1978). Zhuchenko, Korol & Kovtyukh (1985) subjected populations of
D. melanogaster to selection for resistance to extreme temperature fluctuations on
a diurnal scale commencing at a range of 21-29°C which was extended to
15532°C as the experiment progressed. Fifteen generations of selection
considerably increased recombination in the cn-vg region of chromosome 2 and
over the whole b-vg region which encompasses the centromere. Therefore,
selection for resistance to variable temperature stress can lead to a rapid
reorganization of the genetic system of recombination regulation.
60
P. A. PARSONS
'Artificial' situations, such as selection for D D T resistance, provide paradigms
for the study of recombination under a selection regime involving stress. Flexon
& Rodell (1982) selected for resistance to D D T over 555 days increasing the
DDT concentration by a factor of 1900. After 330 days of selection, they studied
recombination levels and found a substantial increase involving chromosomes 2
and 3.
More information is needed in this evolutionarily important area, since the
above results imply that recombination could be increased in the colonization of
marginal habitats where climatic extremes tend to be encountered more
frequently than in the more benign climates expected in more central habitats.
Using 15% ethanol in the culture medium as a stressful environment, Mackay
(1981) set up populations simulating constant environmental conditions, spatial
heterogeneity in the environment, and temporal variation. Additive genetic
variance of sternopleural chaeta number and body weight was greater in
heterogeneous environments than for the constant environment, especially for
temporal variation. I t can be hypothesized that recombination should show
similar responses as argued in discussions of a more theoretical nature (Williams,
1978; Maynard Smith, 1978).
The emphasis upon temperature is not surprising, since at a reductionist level
environmental stress involving temperature can be argued to be an underlying
determinant of adaptation at organizational levels ranging from the
biogeographic to the genetic and molecular. Compared with the other
environmental effects (starvation, nutrition, parental age), temperature effects
are often substantially larger, often by an order of magnitude. I n spite of
quantitative differences, the environmental effects are largely parallel
qualitatively since recombination is generally increased most in centromeric
regions, and more generally the mean and the variability of recombination
increases (Hayman & Parsons, 1960; Lawrence, 1963) under conditions
divergent from any physiological optimum to which populations have become
adapted. At extremes beyond species continuity in the laboratory,
recombination may drop slightly (Fig. I ) . In addition, a sharp decrease in
recombination between 28 and 3 1"C for a temperature-sensitive recombination
deficient allele, rec-P6, in D. melanogaster suggest temperature denaturation of an
enzyme or other protein specified by the mutant and associated with the
recombination process (Grell, 1984). This is a n example of a more general
phenomenon whereby, at temperature extremes, growth rates may be limited by
the rate of a single metabolic reaction so that interpretations in discrete
molecular (and hence genic) terms become increasingly possible in extreme
environments (Langridge, 1963; Parsons, 1986).
At the chromosomal level, a large body of data have been accumulated
supportive of a correlation between chiasmata and genetic crossovers
(Whitehouse, 1965; Peacock, 1968). Comparisons are difficult, since the
assessment of the precise positions of crossovers from recombination experiments
is much more efficient and far more data can be handled. Even so, temperature
influences chiasma frequency in various species of the Acridiidae (White, 1934),
and Henderson (1966) has demonstrated a temperature-sensitive phase in
zygotene-pachytene, some 2 days after DNA synthesis has been completed in
the grasshopper Schistocerca. While there is a tendency for chiasma frequency to
increase with temperature, at the very extreme temperature of 37"C, there is
RECOMBINATION UNDER STRESS
61
evidence for a reduction in chiasma frequency in the grasshopper, Goniaea
australasiae, compared with the control temperature of 26°C (Peacock, 1968).
Similarly, from experiments on a clone of Rhoeo spathacea var. variegata, Lin
(1982) concluded that prolonged exposure to very high temperatures reduces
chiasma frequency.
I n the gekko, Phyllodactylus marmoratus, an experimental study of the male
meiotic system has shown that prolonged exposure to low temperature produces
a significant increase in total chiasma frequency (King & Hayman, 1978).
While it is possible that more extreme cold could reduce total chiasma
frequency, these results show that releasing variability in this manner provides a
high degree of genetic flexibility for a species exposed to environmental
extremes. Cyclic variation on a seasonal basis therefore occurs as also found in
the lizard, Podaris sicula, where an interpretation is provided in terms of sexual
steroid hormones regulating the spermatogenic cycle and to a lesser extent
environmental temperature (Cobror, Olmo, Odierna, Angelini & Ciarcia,
1986).
While more data appear necessary to test the general expectation of more
chiasmata away from a physiological optimum, a consideration of cytological
variables, in particular chiasma frequencies in inbred lines of rye, their Fl’s and
subsequent generations, indicates that these variables are conventional fitness
traits with (in the case of chiasma frequency) some dominance for high
frequency (Rees & Thompson, 1956). Rees (1956) concludes that the proper
working of the chromosomes, like other aspects of the phenotype, depends upon
the maintenance of an optimum degree of hybridity to which a species is
adjusted by natural selection, and which secures a n efficient control of
chromosome behaviour. Any major environmental perturbation will tend to
upset this balance. I n conclusion, the variation in chiasma frequencies offers
interpretations consistent with variation in recombination frequencies, including
reductions under extreme conditions.
GENOMIC AND ENVIRONMENTAL STRESSES: ARE ?‘HEY CUMULATIVE?
There is a substantial literature on the interchromosomal control of
recombination (Lucchesi & Suzuki, 1968) indicating that structural
heterozygosity in one part of the genome usually increases recombination in the
remainder of the genome. In parallel with the environmental variables, the
major effect is in the region of the centromere with a lesser, but marked distal
increase (Schultz & Redfield, 1951). Considering simultaneously heat
treatments of 12 h duration at 35°C and interchromosomal effects (Grell, 1978a)
strikingly similar patterns of response were obtained for recombination (Fig. 4).
An array of hypotheses have been put forward to explain interchromosomal
effects on recombination (Lucchesi & Suzuki, 1968). Given the parallelism with
environmental effects, in particular temperature, any explanation must
encompass both data sets. Schultz & Redfield (1951) put forward the view that
in structurally heterozygous chromosomes some degree of asynapsis may occur,
and this may lead to non-homologous associations exerting stress in regions that
are paired homologously. Lucchesi & Suzuki ( 1968) paraphrase this hypothesis:
“nonhomologous associations disturb the normal attachment or the normal
functioning, or both, of special enzymes, operative in homologously paired
P. A. PARSONS
62
2.5
I
I QSIU//+; UbxI3O/+
,-.
Control
Standard mop distance
Figure 4. Crossing over in five regions of the X chromosome of Drosophila melanogasler after exposure
to heat strcss ( 0 )and to heterozygous inversions in chromosomes 2 and 3 (0).
The graphs give the
relative alteration in crossing over in the X chromosome rxpressed as the ratio experimental/control
(after Grell, 1978a).
regions at the time of crossing over, thereby increasing the probability of
recombination”. The breadth of this genomic stress hypothesis makes it difficult
to test; however, environmental variation would be expected to perturb the
adaptive system implied by this statement, so that any shift away from a normal
environment would be expected to increase recombination. With emphasis upon
temperature, the data discussed in this article can be incorporated into this
model.
I t also follows from the genomic stress hypothesis that other rearrangements
should affect recombination (see Lucchesi, 1976). For example, certain X
chromosome inversions have been found to exert an interchromosomal effect
even when present in the homozygous condition. Such inversions either relocate
a portion of the centric heterochromatin to a position near the distal end of the
chromosome, or the tip of the X to a position near the centric heterochromatin
(Suzuki, 1963). Furthermore, certain autosomal inversions have been found to
enhance recombination when homozygous (Valentin, 1972). Lucchcsi ( 1976)
listed these and other chromosomal and genetic factors that cause
interchromosomal effects on crossing over, and concluded that the most frequent
effect was an increase in levels of recombination with a concomitant reduction
in chromosome interference due to an increase of multiple relative to single cross
overs. Consistent with the hypothesis of Lucchesi & Suzuki (1968) above,
Lucchesi (1976) concludes that “interchromosomal effects do not alter the
process of crossing over per se; rather they reflect alterations in some
precondition(s) for the crossover event”.
Stress can originate from the environment directly or from an alteration at
the cellular level, in particular chromosomal alterations which represent
genomic stresses. McClintock (1978, 1984) has argued for the importance of
stress within the cell and environmental stress imposed from without as triggers
for rapid genomic reorganizations, some of which may occur via mobile genetic
elements, transposons, which are present in the populations of perhaps all
prokaryotic and eukaryotic genomes (Green, 1978; Wills, 1984). Whether
RECOMBINATION UNDER STRESS
63
transposons are involved or not, the hypothesis advanced here is that
environmental stress, genomic stress, or a combination of the two will lead to
enhanced recombination which in D. melanogaster is most pronounced in
centromeric regions. It is often difficult to separate clearly environmental from
genomic stress, simply because the former can lead to the latter.
T h e various stresses could be cumulative for recombination especially as their
regional effects are similar. In D.melanogaster Hayman & Parsons ( 1960) studied
recombination for the three sex-linked genes u, sd and car, for three treatment
contrasts, 20 us. 30"C, age of parent from 0-3 days us. from 4-7 days, and with
and without the heterozygous Cy inversion on chromosomes 2 for the eight
possible treatment combinations made up of the three treatment contrasts. The
Cy inversion increased recombination significantly, and in the younger females
recombination was significantly greater than in the older females. Data for the
segment closest to the centromere, sd-car, are given in Table 3 since this was the
only segment where there was a significant temperature effect, whereby
recombination is greater at 30°C. I n combination with the presence of the
inversion, and for age of female = 0-3 days, flies at 30°C show a substantially
higher recombination percentage than all other treatments (Table 3 ) , the two
extremes being this treatment and the complete opposite, i.e. absence of
inversion, age of female = 4-7 days, and 20°C. The remaining rankings in
Table 3 show the effects of the recombination-increasing variables to be largely
cumulative. Additional experiments would be worthwhile, especially using a
temperature regime where the increase of recombination is higher. This is
emphasized since the effect of 30°C alone (a us. ( 1 ) ) is minor compared with the
effect of 30°C when combined with the inversion and age of females = 0-3 days
(abc us. bc, P<O.10), so that even a mild temperature stress may have substantial
effects upon a system perturbed by other environmental and genetic variables.
From Table 3, the value of abc-( 1) is 5.99, which slightly exceeds the sum of
the three agents promoting recombination taken separately which comes to
5.77, and is more substanially above the product of the separate agents, 4.57, so
that agents promoting recombination in combination could be more than
directly cumulative. Extrapolating from fitness relationships in linkage and in
quantitative genetics experiments, the multiplicative model should be more
realistic biologically (Bodmer & Parsons, 1959; Parsons, 1959). Lucchesi ( 1976)
has pointed out that when two sets of heterozygous inversions are present
simultaneously their combined effect upon recombination tends to be greater
than the sum of their separate effects or their products. A combination of
various environmental and genomic stresses could therefore be associated with
'I'ABLE3. Recombination in the segment sd-car in Drosophila melanogaster with x: values testing for
differences between means (from Hayman & Parsons, 1960)
30°C
20" c
14.52
x:
6.84*
13.43
With
Cy
Without Cy
inversion
inversion
15.29
12.65
37.74**
Age of female
0-3 days
4-7 days
14.91
13.04
26.99**
*P<O.Ol, **P<0.001.
If 'a' represents 30°C, 'b' data with heterozygous Cy inversion, and 'c' age of female from 0 to 3 days, the
ranking oftheeight possible treatment combinations is: abc (17.22) l a b (15.64) >bc (15.00) > c (14.18) > b
(13.30) > a c (13.23) > a (11.98) > ( I ) (11.23).
64
P. A. PARSONS
recombination at levels exceeding their individual effects, so that some
combinations of genomic and environmental stress agents may generate
variability permissive of rapid adaptation to novel conditions.
Assessing the evolutionary consequences of genomic and environmental
stresses in nature is a problem of central importance. However, relationships
with habitats and climates need to be established, which is difficult because
periods of extreme stress may be quite short. Such short periods are a feature of
many habitats, for example the resource-specific species D.hibisci (Parsons,
1981) may be exposed to temperatures exceeding 35" for a few hours during the
day, dependent upon precise weather conditions. I n addition to adults, larvae,
and especially pupae, may be subjected to periods of high stress, so that
comparative experiments across life cycle stages are needed, especially given the
sensitivity of certain larval developmental stages to the effects of severe heat
stress in promoting increased recombination. I n attempting to extrapolate to
nature, maximum recombination is likely under stress conditions approaching
lethality. As argued in Parsons (1986), this applies to evolutionary rates in
general since this is the time of high genotypic and phenotypic variability of all
forms. This paper forms an attempt to incorporate recombination into this
wider scenario.
Much has been written on recombination a t the enzyme and protein level.
Apart from the passing comments presented, a detailed consideration of this
literature would detract from the emphasis presented concerning ecological
variables involving stress. A general feature of stressed systems at the metabolic
level is an increase in energy expenditure, since following a severe perturbation
energy is diverted from maintenance and production to repair and recovery
(Odum, 1981). One measure of the metabolic energy available to an organism
at a given time is the adenylate energy charge (AEC) expressed as the ratio
[ATP] ++[ADPI
[ATP] [ADP] [AMP] '
+
+
where [ATP], [ADP] and [AMP] represent amounts of adenosine triphosphate,
diphosphate and monophosphate respectively (Atkinson, 1977). The AEC is a
measure of the useful energy stored in the adenylate system. Stresses of the types
emphasized in this paper where viability losses may be apparent even following
a return to normal conditions give AECs of about 0.5, compared with 0.8-0.9
under optimal conditions (Ivanovici & Weibe, 1981). Based upon the generality
of stresses affecting AECs in this way, it is therefore likely that the stresses
increasing recombination would normally correspond to AECs at the low end of
the viable range. Furthermore, it follows that stressful agents promoting
recombination would be at least cumulative in their effects. Indeed synergism,
as suggested above for the combination of genomic and enviromental stresses, is
likely since responses of AECs to stresses appear to be non-linear, whereby for
small increments of environmental factors, a relatively large decrease in AEC is
found when conditions cross a suboptimal threshold (Ivanovici & Weibe, 1981).
Given the pivotal importance of adenylates in metabolism, in particular ATP,
experiments are needed to explore the effects upon recombination of variable
AEC levels resulting from stresses singly and in combination. This derives from
the apparent role of the AEC level as a metabolic indicator of the relative
severity of an ecological stress.
RECOMBINATION UNDER STRESS
65
ACKNOWLEDGEMENTS
I am grateful to R. W. Allard, R. J. Berry, and M. M. Green for discussion
on “stress and recombination”. In particular, I wish to thank A. A. Hoffmann
for a careful review of the manuscript; the last paragraph will be more fully
developed in a joint paper with him which is being prepared for The
Bicentenary Symposium of the Linnean Society on Evolution, Ecology and
Environmental Stress.
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