Evolution of Genome Size in Drosophila. Is the Invader’s Genome Being
Invaded by Transposable Elements?
Cristina Vieira,* Christiane Nardon,* Christophe Arpin,† David Lepetit,* and
Christian Biémont*
*Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Lyon 1, Villeurbanne Cedex, France; and
†INSERM-U503, CERVI, Lyon Cedex 07, France
Genome size varies considerably between species, and transposable elements (TEs) are known to play an important
role in this variability. However, it is far from clear whether TEs are involved in genome size differences between
populations within a given species. We show here that in Drosophila melanogaster and Drosophila simulans the
size of the genome varies among populations and is correlated with the TE copy number on the chromosome arms.
The TEs embedded within the heterochromatin do not seem to be involved directly in this phenomenon, although
they may contribute to differences in genome size. Furthermore, genome size and TE content variations parallel
the worldwide colonization of D. melanogaster species. No such relationship exists for the more recently dispersed
D. simulans species, which indicates that a quantitative increase in the TEs in local populations and fly migration
are sufficient to account for the increase in genome size, with no need for an adaptation hypothesis.
Introduction
Genome size (the C-value) is known to vary considerably among organisms but is relatively constant
among individuals of the same species (Mirsky and Ris
1951), and its significant degree of variation among organisms, more than 200,000-fold among eukaryotes
(Gregory 2001), is not linked to biological complexity
(Petrov 2001). Several hypotheses have been proposed
to explain this genome size variation. The ‘‘selfish
DNA’’ hypothesis suggests that the accumulation of
DNA over evolutionary time may result from the cell
replication process. The increase in genome size thus
ceases when it begins to compromise cell viability (Doolittle and Sapienza 1980; Orgel and Crick 1980; Pagel
and Johnston 1992). According to this theory, larger
cells can simply tolerate more DNA (Gregory 2000). An
alternative hypothesis postulates that genome size may
influence the fitness of the organism by a nucleoskeletal
effect that is based on the amount of nuclear DNA and
is independent of the nucleotide sequence. According to
this hypothesis, genome size is considered to be a selective trait because larger cells will need larger nuclei
to preserve a favorable metabolic balance (CavalierSmith 1978, 1985, pp. 253–265; Cavalier-Smith and
Beaton 1999). This relationship implies an inverse correlation between genome size and some life history
traits, such as the rate of cell division (Cavalier-Smith
1985), metabolism (Vinogradov 1995, 1997), and development (Sessions and Larson 1987), with natural selection acting on the global phenotype of the organism.
Both hypotheses relate the increase of genome size to
cell volume, but their interpretations are strikingly different (see Gregory and Hebert 1999 for a review). In
addition to these correlations, several studies have also
identified relationships between genome size and cliKey words: genome size, Drosophila, transposable elements.
Address for correspondence and reprints: Cristina Vieira, Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, 43 bd
11 novembre, Université Lyon 1, 69622 Villeurbanne Cedex, France.
E-mail: [email protected].
Mol. Biol. Evol. 19(7):1154–1161. 2002
q 2002 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038
1154
mate. Hence, some fishes (Beaton and Hebert 1988),
salamanders (Xia 1995; Jockush 1997), and several
plants (Grime and Mowforth 1982; Kalendar et al. 2000;
Tarchini et al. 2000) from high latitude and altitude exhibit larger genomes and more frequent polyploidy than
species from low latitude and altitude.
Genome size variability is usually attributed to differences in the amount of repetitive DNA, which corresponds to a large fraction of the genome (Pagel and
Johnston 1992). For example, the human genome consists of only 5% of coding sequences but more than 40%
of transposable elements (TEs) (International Human
Genome Sequencing Consortium 2001). A link between
genome size and the amount of TEs is therefore to be
expected. Recent data provide evidence that the TE copy
number is related to environmental conditions and to the
colonization process (Arnault and Dufournel 1994; Labrador and Fontdevila 1994; Wisotzkey, Felger, and Hunt
1997; Labrador et al. 1999). Kalendar et al. (2000) have
shown that the Bare-1 element in barley, is responsible
for a large genome size variation, and its copy number
increases in relation to the height and dryness of the
environment. An association between genome size variation and TE content has also been found in rice, which
contains 14% of LTR retrotransposons (Tarchini et al.
2000). An increase in the genome size of maize is the
result of recent TE amplifications, which have occurred
within the last 2 to 6 Myr (SanMiguel and Bennetzen
1998). TEs may also contribute to an increase in genome
size after crosses between different species. This was
observed when two wallaby species, Macropus eugenii
and Wallabia bicolor, were crossed (O’Neill, O’Neill,
and Graves 1998). The centromeric regions of the hybrids were amplified, and the amplified sequences presented homologies to human endogenous retroviral elements. In Drosophila, crosses between Drosophila buzzatti and D. koepferae mobilize the osvaldo element in
hybrids (Labrador and Fontdevila 1994; Labrador et al.
1999).
Most of the work done on genome size is based on
comparisons between different species. However, the
few studies which have been done at the population lev-
Genome Size and Transposable Elements
el reveal differences in genome size between populations in mammals, such as the pocket Gophers (Sherwod
and Patton 1982), fishes (Gold and Amemiya 1987;
Gold, Ragland, and Schliesling 1990; Lockwood and
Derr 1990), and insects, such as mosquitoes (Rao and
Rai 1987; Black and Rai 1988; Warren and Crampton
1991) and Drosophila (Dawley 1997, pp. 143–184). One
way to explain these intraspecific differences is to view
genome size as a selective trait (Gregory 2001). An alternative hypothesis, however, is that TEs may be mobilized under stressful environmental conditions (Arnault and Dufournel 1994) or genetic conditions (Wisotzkey, Felger, and Hunt 1997; Biémont et al. 1999;
Labrador et al. 1999), in some cases after horizontal
transfer (Kidwell and Lish 1997). As a consequence, the
colonization of new habitats could lead to the mobilization of certain TEs in the genome of invasive species,
leading to an increase in genome size. In the present
study we used flow cytometry to estimate genome size
of individuals from various geographically distinct populations of D. melanogaster and D. simulans, and we
correlated genome size with the total amount of TEs
previously estimated by in situ hybridization (Biémont
et al. 1999; Vieira et al. 1999). We show that differences
in TE amount in the euchromatic part of the chromosomes do indeed account for some of the differences in
genome size between species and between populations
within a given species. The amount of TEs in centromeric heterochromatin does not seem to be involved in
this correlation in a simple way.
Materials and Methods
Natural Populations
We worked on fly samples collected from several
geographically distinct natural populations. The D. melanogaster populations considered were from Arabia,
Argentina (Virasoro), Bolivia, China (Canton), Congo
(Brazzaville), France (St Cyprien), Portugal (Chicharo),
Réunion Island, Senegal, and USA (Seattle). The populations of D. simulans were from Australia (Canberra,
Cann River, Eden), France (Valence), Kenya (Makindu),
Madagascar, New Caledonia (Amieu), Polynesia (Noumea, Papeete), Portugal (Madeira), Réunion Island, Russia (Moscow), and Zimbabwe. These populations were
maintained in the laboratory at 188C as isofemale lines
or small mass cultures with around 50 pairs in each
generation.
Estimation of the Euchromatic TE Copy Number
The
mosomes
ments in
(Biémont
TE insertion site number of polytene chrohad previously been determined for 31 elesamples of the populations described above
et al. 1999; Vieira et al. 1999).
Estimation of the Total Amount of TEs
We estimated the relative total amount of each TE
individually by an inverse dot blot technique, which was
developed by D. Lepetit. One microgram of each plasmidic DNA containing a TE sequence and 1 mg of actin
1155
Table 1
Average Copy Numbers of TEs Per Diploid Genome on
Euchromatin Determined by In Situ Hybridization
DROSOPHILA
MELANOGASTER
TEs
Canton
Senegal
17.6 . . . . . . . . . . .
297 . . . . . . . . . . . .
412 . . . . . . . . . . . .
17.31 . . . . . . . . . .
bari-1 . . . . . . . . . .
bell . . . . . . . . . . . .
blood . . . . . . . . . .
burdock . . . . . . . .
copia . . . . . . . . . .
coral. . . . . . . . . . .
doc . . . . . . . . . . . .
F. . . . . . . . . . . . . .
Flea . . . . . . . . . . .
gypsy . . . . . . . . . .
helena. . . . . . . . . .
HMS-Beagle . . . .
hobo . . . . . . . . . . .
I ..............
idefix. . . . . . . . . . .
jockey . . . . . . . . . .
mariner . . . . . . . .
mdg1 . . . . . . . . . .
mdg3 . . . . . . . . . .
nomade . . . . . . . .
opus . . . . . . . . . . .
pogo . . . . . . . . . . .
roo/B104 . . . . . . .
springer . . . . . . . .
stalker . . . . . . . . .
tirant . . . . . . . . . .
zam. . . . . . . . . . . .
6.5
26.5
24.0
2.5
8.0
7.5
22.5
11
28.5
19.5
24.5
41
15
1.5
0
13.5
54.5
22.5
5
36
0
21
17
20
22.5
14
62.5
2.5
14
10.5
0.5
0.5
16
25.5
1.5
5
8.5
16
9
20
9
23
16
11
0.5
0
9
41
25
6
24
0
16.5
9
14
18.5
10
44.5
1.5
5.5
8.5
0
DROSOPHILA SIMULANS
Canberra Madagascar
0
1
59.5
1.5
3.5
0
1
3.5
4
3
19
10.5
1.5
3
10
2.5
63.5
18
1
1
7.5
0
4.5
7.5
8.5
0
47.5
0
0
1
0
0
0
5.5
1
4.5
1
2.5
2
3
0
11
0
2.5
2
9
11
56
10
1
4.5
2
0
1.5
0
4
0
28.5
0
0
1
0
DNA used as control were blotted on a nylon N1 membrane (Amersham). The membrane was hybridized with
100 ng of DNA extracted by classical technique from
20 adult female flies from a given population. This DNA
was sonicated, and the resulting fragments were labeled
with 32P dCTP by random priming. The same blot was
thus hybridized successively with the DNA from four
different populations, Canton and Senegal for D. melanogaster and Canberra and Madagascar for D. simulans.
The list of the TEs used in the dot blot experiment and
their euchromatic copy number determined by in situ
hybridization are given in table 1. Autoradiographic signal intensity was acquired with the Molecular Imager
System, analyzed with Biorad Molecular Analyst R System and Biorad software, and adjusted as a function of
the actin activity. Because the labeling of the probe by
random priming is not independent of the base composition, we considered the ratio between populations for
each TE. This hybridization with whole fly DNA made
it possible to estimate the amount of heterochromatic
and euchromatic copies for each TE. In comparison, in
situ hybridization gave only the number of TE insertion
sites distributed along the euchromatic part of the chromosomes; therefore, it was an underestimation of the
real TE copy number because each site labeled could in
fact bear more than one TE copy.
1156
Vieira et al.
Estimation of the Genome Size
Nuclei were extracted from five heads of 5- to 10day-old males or females. The heads were crushed in a
small, siliconized Eppendorf vial containing 200 ml labeling solution (0.1 g trisodium citrate, 0.01 ml Triton
X-100, 0.05 mg RNAse-A, water UHQ 100 ml, following R. Dawley, personal communication) with 1 mg/ml
propidium iodide (Aldrich). Tetraodon (Tetraodon nigroviridis) blood was used as the internal standard for
diploid genome size (0.8 pg). In order to distinguish
between this standard and the fly head nuclei, the tetraodon blood was labeled with the fluorescent dye 5and 6-carboxyfluorescein diacetate succinimidyl ester
(CFSE, Molecular Probes) at 2 mg/ml in PBS for 15
min, at 378C. The reaction was blocked by adding an
excess of proteins in the form of an equal volume of
cold fetal calf serum. Twenty microlitres of stained tetraodon blood was then added to the solution of fly head
nuclei. The final mixture thus contained similar amounts
of blood cells and fly nuclei, as estimated using a Thoma
nucleus-counting cell. The mixture was incubated for 10
min in ice and filtered across 140 mm and then 30 mm
nylon meshes. Six-hundred microlitres of initial labeling
solution was then added to achieve an appropriate dilution. The resulting solution was analyzed on a FACScalibur flow cytometer (Becton Dickinson Instruments)
fitted with an argon laser at 488 nm wavelength. About
20,000 nuclei were analyzed, with an average rate of
300 events/s for each determination of the genome size
of the flies. Genome sizes were estimated for the 10
populations of D. melanogaster or the 13 populations of
D. simulans simultaneously, and the experiment was
replicated four times for males and four times for females, independently. Flow cytometry, which is commonly used in the medical field and in plant biology,
provides an accurate determination of differences in genome size (Ulrich 1990; Michaelson et al. 1991; Lauzon
et al. 2000) and is considered to be highly reliable for
detecting tiny differences in genome size, such as a difference of 1.5% (Kent, Chandler, and Wachtel 1988). An
example of a flow cytometry analysis of one sample of
fly head nuclei and tetraodon blood is shown in figure 1.
Results
Genome Size Variation
Two-way analysis of variance was performed to detect the effects of sex and population in each species
(see tables 2 and 3). There was no significant difference
in mean genome size between males (0.395 6 3.8 3
1025 pg) and females (0.394 6 7.4 3 1025 pg) for D.
melanogaster. However, in D. simulans, the males had
a bigger genome (0.356 6 3.4 3 1025 pg) than the females (0.348 6 3.3 3 1025 pg). Significant differences
were also detected between populations within each species (see tables 2 and 3).
Euchromatic TE Amount and Genome Size
As the genome size was significantly different in
different populations, we investigated whether there was
any correlation between genome size and the total
amount of TEs on the polytene chromosomes. Figure 2
shows significant linear correlations and regressions between genome size and the TE insertion site numbers
of males and females for the 10 populations of D. melanogaster and the 13 populations of D. simulans. Drosophila melanogaster had a larger genome than D. simulans and also displayed a stronger correlation between genome size and TE copy number.
The difference observed between the two species
for their TE amount, the correlation between genome
size and TE copy number between populations within
the same species, and our experimental protocol, makes
it unlikely that differences in DNA stainability could
account for differences in genome size between populations. Changes in chromatin structure or chromatin
condensation could have indeed lead to a wrong estimation of genome size because the DNA fluorescence
would be incorrect (Noirot et al. 2000). However, this
was unlikely in the present study because there is no
reason to suppose that the different populations would
have different levels of chromatin condensation associated with their TE copy number.
Contribution of TEs to Genome Size Variation
To determine the contribution of the TEs to genome
size variation, we estimated the amount of TEs in picograms for the populations of extreme genome size for
both species (Canton and Senegal for D. melanogaster;
Canberra and Madagascar for D. simulans). The number
of copies of each TE, estimated by in situ hybridization
(table 1), was multiplied by the TE length in pg (1 pg
equals 0.9869 3 109 bp). The difference in TE amount
between the two extreme genome size populations within each species was then expressed as a percent of the
genome size difference. It appears that variations in TE
copy number in euchromatin account for only 5% to 9%
of the observed difference in genome size. Other factors,
such as the proportion of repetitive sequences in heterochromatin or the interspersion of highly repetitive DNA
in the genome, must be involved to account for the difference in genome size, for which the TE copy number
seems to be a distinctive label. We thus determined by
dot blot the total amount of TEs in the heterochromatic
and euchromatic parts of the genome of whole flies from
the two populations with extreme size in each species
(see an example of dot blot in fig. 3). In D. simulans,
the ratio of the blot intensities from whole DNA between Canberra and Madagascar was equal to 1.10,
whereas the ratio of the copy number estimated by the
in situ technique was equal to 1.72 (the TEs with no
insertion sites were excluded from the calculus). If we
removed the 412 element from the calculation (the element that is overrepresented in the Canberra population), the dot blot and the in situ techniques gave copy
number ratios between Canberra and Madagascar equal
to 1.03 and 1.34, respectively. This shows that the Canberra and Madagascar populations did not differ significantly when the total genomic amount of TEs was considered. The number of insertion sites on the chromo-
Genome Size and Transposable Elements
1157
FIG. 1.—Example of flow cytometry analysis of nuclei samples. (A) Dual FL3-width/FL-3-area plot was used to eliminate nuclei doublets
from the analysis (R1). (B) Dual FL1-H/FL-3H plot analysis was used to separate fly nuclei (R2) and the tetraodon blood internal standard
(R3). A threshold was set on FL3-H to eliminate cell debris from the analysis. (C) FL3-H fluorescence distribution of propidium iodide–stained
DNA samples from tetraodon internal control (R1 and R2) and fly head nuclei (R2 and R3). The two peaks observed in the fluorescence profile
of fly nuclei DNA correspond to the diploid (M1) and tetraploid (M2) nuclei. The mean FL3-H fluorescence from diploid fly nuclei and from
tetraodon blood nuclei was used to calculate the Drosophila genome size of each sample.
some arms was thus not associated with the amount of
TEs within the heterochromatin. It is thus the variation
in the number of insertion sites along the chromosomes
which was responsible for the main variation in total
amount of TEs in D. simulans. This conclusion is sustained by the strong correlation between the ratios of the
dot intensity and the in situ insertion site number of
Canberra over Madagascar (r 5 0.895, P , 0.0001).
Table 2
ANOVA of Genome Size in Populations of D.
melanogaster
Source of Variation
Sex . . . . . . . . . . . . . . .
Population. . . . . . . . . .
Sex 3 population. . . .
Error . . . . . . . . . . . . . .
df
Mean Square
1
9
9
60
3
3
3
3
4.24
2.16
4.61
3.34
25
10
1024
1025
1025
F
1.27
6.46
1.38
NOTE.—NS, not significant, P . 0.05; *** P , 0.001.
Again, when we excluded the 412 element from the
analysis, the correlation dropped to r 5 0.693 but was
still significant (P , 0.01) (fig. 4). Drosophila melanogaster presented a different picture. The ratios of the
most extreme populations for genome size, Canton and
Senegal, were equal to 1.24 and 1.36 for the dot blot
and the in situ hybridization techniques, respectively.
This suggests that (1) the TE insertions on the euchromatin, to a great extent, determine the total amount of
Table 3
ANOVA of Genome Size in Populations of D. simulans
P
NS
***
NS
Source of Variation
Sex . . . . . . . . . . . . . . .
Population. . . . . . . . . .
Sex 3 population. . . .
Error . . . . . . . . . . . . . .
df
Mean Square
F
P
1
12
12
78
3
3
3
3
73.40
3.06
1.67
***
***
NS
1.85
7.70
4.21
2.52
23
10
1025
1025
1025
NOTE.—NS, not significant, P . 0.05; *** P , 0.001.
1158
Vieira et al.
FIG. 3.—Dot blot obtained for the two populations with extreme
genome size for D. simulans (see Materials and Methods for the technical procedure). Spots from left to right: 17.6, 297, 412, 1731, Bari1, Bell, blood, burdock, copia, coral, Doc, F, Flea, gypsy, HMS Beagle, hobo, I, Idefixe, jockey, mdg1, mdg3, mariner, nomade, opus,
pogo, roo/B104, springer, stalker, tirant, Zam, actine. Mk—Madagascar, Cb—Canberra.
FIG. 2.—Genome size (pg) versus number of insertion sites of
TEs along the chromosomes. (a) males of D. simulans (black circles)
and D. melanogaster (white circles), (b) females of D. simulans (black
circles) and D. melanogaster (white circles). Linear correlation coefficients: Drosophila melanogaster, r 5 0.55, P , 0.05 for males; r 5
0.67, P , 0.001 for females; D. simulans, r 5 0.40, P , 0.01 for
males; r 5 0.42, P , 0.01 for females. The regression lines for males
correspond to Y 5 0.339 1 0.000043 X for D. simulans, and Y 5
0.358 1 0.000036 X for D. melanogaster. The regression lines for
females correspond to Y 5 0.330 1 0.000045 X for D. simulans and
Y 5 0.331 1 0.000061 X for D. melanogaster. The variable Y is
genome size (pg) and X the TE insertion site number.
observation that the genome of D. melanogaster contains more middle repetitive DNA than that of D. simulans (Dowsett and Young 1982; Vieira et al. 1999).
We have previously shown that D. melanogaster populations from Africa (the cradle of this species) harbor a
low total amount of TEs but that this amount increases
in populations from other continents. We therefore suggested that TE acquisition and accumulation may parallel the D. melanogaster colonization process (Vieira
et al. 1999). We show here that genome size variation
in the D. melanogaster populations is correlated with
the TE amount; thus, it also parallels the species colonization. No global association between geographic distribution of populations and the overall TE amount was
observed in D. simulans populations (Vieira et al. 1999),
TEs, (2) the amount of TEs in heterochromatin parallels
the amount on euchromatin, or (3) in Canton, the TE
amount on heterochromatin increased, whereas it varied
independently of the insertion site number in euchromatin. The first hypothesis can be discounted because
the ratio of the total genomic amount of eight TEs with
very low insertion sites determined by in situ was equal
to 1.47 and thus did not differ from the value obtained
when all TEs were considered. The second hypothesis
can be eliminated because correlation between the ratios
of dot blot intensity and the in situ insertion site number
of Canton and Senegal (r 5 20.13) (fig. 4) was low
and nonsignificant, in contrast with that in D. simulans.
This suggests that the TE amount within heterochromatin was higher in Canton than in Senegal and that
this TE amount in heterochromatin increased from Senegal to Canton independent of the increase in insertion
sites on euchromatin, as proposed by the third
hypothesis.
Discussion
The fact that the genome of D. melanogaster is
larger than that of D. simulans concurs with the usual
FIG. 4.—Dot blot versus in situ hybridization ratios of TE amount
in populations with extreme genome size for (a) D. melanogaster and
(b) D. simulans (see text for the correlation values).
Genome Size and Transposable Elements
and the correlation between TE amount and genome size
is lower than that in D. melanogaster. This lower level
of correlation is attributed to the fact that certain populations of D. simulans have a high copy number of
some TEs but not of others, whereas populations of D.
melanogaster have high copy number for most TEs (Vieira et al. 1999). Indeed, for most populations of D.
simulans, any increase in the copy number for one or
only a few TEs is not sufficient to influence genome
size significantly. However, the Canberra population of
D. simulans has the largest genome in the species and
has a significantly larger number of copies of most TEs,
especially when compared with the Madagascar population, which has small genome size and a low TE copy
number (Vieira, Piganeau, and Biémont 2000). The main
point that emerged from these findings is that the TE
insertion site number on chromosome arms (the euchromatic copies) only contributes to about 5% to 9% of the
observed genome size variations. This suggests that genome size variation is caused by other factors as well
as by the TEs in euchromatin. TE copies and blocks of
complex DNA embedded in the heterochromatic regions
of the chromocenter are good candidates for explaining
such differences in genome size (Vaury, Bucheton, and
Pélisson 1989; Miklos and Cotsell 1990; Nurminsky et
al. 1994; Le, Duricka, and Karpen 1995). We have
shown in D. melanogaster that the variation in the TE
amount within heterochromatin does not follow the variation in TE number in euchromatin when TEs are considered individually, although the Canton population
with a high genome size has both a high amount of TEs
within heterochromatin and high TE insertion site numbers in euchromatin. We must therefore envisage that
the amplification of other repetitive sequences in heterochromatin or euchromatin may be associated in one way
or another with the TE copy number on chromosome
arms. For example, in plants it is the size of repetitive
blocks between genes that correlates with genome size
(Chen et al. 1997), and amplification and deletion of
satellite DNA has been observed in many species (Csink
and Henikoff 1998; Slamovits et al. 2001), all phenomena which could have involved chromatin remodeling
(Henikoff, Ahmad, and Malik 2001). The fact that D.
simulans males have bigger genomes than females may
indicate a specific increase of repeated sequences in the
heterochromatin of the Y chromosome of that species.
Historical processes have led to the invasion of the
D. melanogaster genome by many TEs a long time ago,
apart from the P and I elements, which only invaded
this species at the beginning of the 1900s. In contrast,
populations of the D. simulans species still seem to be
in the process of being invaded by TEs (Vieira et al.
1999). Increases in genome size could therefore result
from an increase in TE copy number, which could result
from mobilization of TEs induced by environmental
stresses, as has been reported in bacteria, yeast, and
plants (Newton, Wakamiya, and Price 1993, pp. 321–
345; Arnault and Dufournel 1994; Kidwell and Lish
1997). When populations are subjected to new environmental conditions, as may happen in populations that
have invaded novel habitats, some of their TEs may be
1159
mobilized (Capy et al. 2000; Kalendar et al. 2000) and
their genome size increased, leading to the observation
that genome size increases during geographical colonization (Cros et al. 1995). Drosophila melanogaster and
D. simulans both originated in East Africa (Lachaise et
al. 1988), and the relationship between genome size and
geography in D. melanogaster could therefore mainly
reflect the geographic distance from the African birthplace, rather than any adaptive process. The high copy
number of the uhu and LOA elements in Hawaiian Drosophila suggests that the colonization of new islands
from older islands may have been associated with a significant increase in TE copy number (Wisotzkey, Felger,
and Hunt 1997). The unusual distribution of the osvaldo
element in populations from the Iberian Peninsula compared with the original populations in Argentina (Labrador et al. 1999) also implies an association between
an increase in TE copies and colonization processes. TE
transposition has also been seen to increase in both Drosophila hybrids (Evgen’ev et al. 1982; Labrador et al.
1999) and in the hybrid Australian wallaby (O’Neill,
O’Neill, and Graves 1998), resulting from confronting
populations or species that did not previously overlap.
We still have much to learn about the genome. This
paper and other recent studies on Drosophila, plants,
fishes, and yeast, should trigger a fresh debate on genome changes associated with species invasion of new
habitats, geographical locations, and evolution. Progress
in this area of research can benefit from the comparative
analysis of genomes of native and newly derived populations of the numerous pest species that are continually invading new areas of our world. The Zebra mussel,
cheatgrass, European house sparrow, Argentine ant (Orr
and Smith 1998; Duke and Mooney 1999; Duvernell
and Turner 1999), and many other invaders, in addition
to the more common Drosophila species, should help us
to understand the link between chromatin structure, TE
mobilization, genome size, success of colonization, and
various adaptive characteristics.
Acknowledgments
We would like to thank J. Marvel, R. Dawley, and
J. S. Johnston for their advice on the flow cytometry
analysis of fly nuclei, C. Fisher for her gift of Tetraodon
blood, and R. Grantham and C. Loevenbruck for their
help. This work was funded by the Centre National de
la Recherche Scientifique and the Association pour la
Recherche sur le Cancer. We thank M. Ghosh for reviewing the English text.
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PIERRE CAPY, reviewing editor
Accepted March 5, 2002