Genetica 105: 43–62, 1999. © 1999 Kluwer Academic Publishers. Printed in the Netherlands.
43
Distribution of transposable elements in Drosophila species Christian Bi´emont & G´eraldine Cizeron Laboratoire de Biom´etrie, G´en´etique, Biologie des Populations, UMR C.N.R.S. 5558, Universit´e Lyon 1, 69622 Villeurbanne, France (Phone: (33) 4 72 44 81 98; Fax: (33) 4 78 89 27 19; E-mail:
[email protected]) Received 5 January 1999 Accepted 3 February 1999
Key words: distribution, Drosophila, retrotransposon, transposable element
Abstract We present a global analysis of the distribution of 43 transposable elements (TEs) in 228 species of the Drosophila genus from our data and data from the literature. Data on chromosome localization come from in situ hybridization and presence/absence of the elements from southern analyses. This analysis shows great differences between TE distributions, even among closely related species. Some TEs are distributed according to the phylogeny of their host species; others do not entirely follow the phylogeny, suggesting horizontal transfers. A higher number of insertion sites for most TEs in the genome of D. melanogaster is observed when compared with that in D. simulans. This suggests either intrinsic differences in genomic characteristics between the two species, or the influence of differing effective population sizes, although biases due to the use of TE probes coming mostly from D. melanogaster and to the way TEs are initially detected in species cannot be ruled out. Data on TEs more specific to the species under consideration are necessary for a better understanding of their distribution in organisms and populations. Introduction Transposable elements (TEs), by virtue of their capacity of invading the genome and promoting mutations, recombination and even conversion (ThompsonStewart, Karpen & Spradling, 1994; Smit, 1996), are a serious threat to the genome. Although they may have played a major role in evolution and may still be useful in maintaining the genetic variability of natural populations, the way they invade genomes and how their copy number is contained in genomes and populations are still matters of great debate. To understand TE dynamics and estimate their possible effects on evolution, we need data on their copy number and genomic localization in different species. Although data on TE genomic distributions are now available from various organisms, including plants (HeslopHarrison et al., 1997) and mammals (Löwer, Löwer & Kurth, 1996; Patience, Wilkinson & Weiss, 1997), the main source of information comes from Drosophila, especially Drosophila melanogaster. Two large analyses of the distribution of mobile elements in the genus Drosophila were previ-
ously published (Martin, Wiernasz & Schedl, 1983; Stacey et al., 1986). These studies concerned the elements copia, 412, 297 and three other not-wellknown middle repetitive sequences in 32 species in Martin, Wiernasz and Schedl (1983), and the elements P, I, gypsy, copia and F in 34 species in Stacey et al. (1986). Since then many data have been accumulated, and the present paper summarizes data from 228 species of the genus Drosophila and 43 TEs including retrotransposons (copia-like, gypsy-like and related elements), retroposons (nonLTR retrotransposons: I-like elements), transposons (P- and Tc-like elements) and a foldback element. More elements in even more species could have been included, but we have limited our investigation to the elements for which information on presence/absence was available in more than one species or for which the number of euchromatic insertion sites in the entire genome was determined. The analysis reveals great differences in distribution between TEs, but the data are subjected to many biases which are discussed.
44 Materials and methods Data on chromosome localization come from in situ hybridization, and data on presence/absence of the elements from southern analyses; the data come from the literature. Most of the studies on TE distribution were done on D. melanogaster and the seven other species belonging to the melanogaster subgroup of the subgenus Sophophora. Many TEs are specific to these species and we have a large amount of data on their euchromatic insertion site numbers. Thus, we have presented in Tables 1 and 2 the data set corresponding to the melanogaster species subgroup, and in Tables 4–13 the data from other species of the genus Drosophila, grouped according to the TEs classes and the taxonomic subgroups. We have not included on the tables the presence of elements in the heterochromatic regions because this information is not available for all the TEs and species. The table with the complete set of data (as a Microsoft Excel spreadsheet) can be obtained upon request from the authors.
The melanogaster species subgroup The main characteristic from Table 1 is the similar number of copies observed for many different elements in D. melanogaster, whatever the family of TEs (retrotransposons, retroposons or transposons) concerned. Indeed, many TEs have average copy numbers ranging from 10 to 30. However, some elements, like the gypsy retrotransposon, possess only 0–2 copies on the chromosome arms, and the roo/B104 retrotransposon has around 100 copies. The general picture is similar in D. simulans except that this species seems to have lower numbers of copies per element for most of the TEs (Leibovitch et al., 1992; Nuzhdin, 1995; Vieira & Biémont, 1996b). To see whether this apparent lower copy number of TE insertions is compatible with the classical observation that D. simulans carries approximately three times less middle repetitive DNA than D. melanogaster (Dowsett & Young, 1982), we have presented on Table 3 the raw data from natural populations, laboratory strains, and lines available in the literature and extracted from Tables 1 and 2 for the insertion site numbers of those TEs for which data were informative. Although these data are very crude, it is striking to observe an average ratio (averaged over TEs) of the number of TE insertions in D. melanogaster to numbers in D. simulans equal to 3.06 (standard deviation: 2.39) and an overall number of insertion
sites in D. melanogaster over that in D. simulans equal to 1.95 (387.9/199.2), both values compatible with the above crude ratio of overall amount of middle repetitive DNA in these two species. From Table 3 it appears, however, that all TEs do not follow this general picture. Indeed nine TEs of the 17 considered have a ratio less than 2.0. TEs such as gypsy, doc, hobo, bari-1 and FB have similar numbers of insertions in both species, while copia, jockey, F and opus have many more insertions in D. melanogaster than in D. simulans. To evaluate this crude observation (do these classes of elements : LTR retrotransposons, nonLTR retrotransposons, transposons, reflect the same numerical tendency?), we need more reliable data on distributions of many TEs in natural populations for both D. simulans and D. melanogaster. The fact that D. simulans seems to have fewer copies overall of most TEs in its chromosome arms than does D. melanogaster might reflect some specific evolutionary features of the D. simulans genome that have the effect of restraining the number of TE sequences in this species (Kimura & Kidwell, 1994), or might only be due to a melanogaster-bias in the sampling. A striking observation, however, is the high copy numbers of the 412 and roo/B104 retrotransposons that have been reported in some populations of D. simulans (Vieira & Biémont, 1996b; Vieira et al., 1998). These high values, which are similar to those of D. melanogaster, reflect specific characteristics either of these populations or of the environmental conditions surrounding the populations and which could interfere with the copy number regulation, as reported recently for the 412 element in D. simulans (Vieira et al., 1998). Do these high values mean that D. simulans will be invaded by many TEs in the near future and will acquire copy numbers similar to those of D. melanogaster? And will such a phenomenon be dependent upon the present world-wide spread of D. simulans (Hyytia et al., 1985; Singh, Choudhary & David, 1987; Singh, 1989; Capy, Pla & David, 1993)? Studies of other elements, that have also some copies scattered over the chromosome arms, are necessary to better ascertain the distribution of TEs in natural populations of D. simulans. If such studies lead to the discovery of a natural population with high copy numbers for specific TE(s), we would then possess powerful material to search for the specific genomic properties controlling TE copy numbers in natural populations. In the same way, we should analyse other species living under different natural conditions and with different effective population sizes in order to evaluate the real influ-
0.0 3.0 3.4 4.0 2.5 4.0 1.0− 0w− 0+ 0+
simulans
mauritiana sechellia yakuba teissieri erecta orena
0.6 3.0 12.0
16.8 17.6 17.7 19.4 20.0 21.2 24.0 24.5 30.0 14–27
mdg-1b
1.0 3.0 5.0
12.0 12.5 8.5 8.5 5–18
mdg-3c
3.0 2–3 0+ 0+ 0+ 0+
3.7 14.2 19.0
14.7 16.1 20.6 25.3 29.7 31.1 32.4
412d
2.0 1.0
0–5
0–3 10.4
1731e
1.0 1.6 2–3
0.9 0–5 2–3 1.0 1.4 20–50
gypsyf
28–43
12.5
17.6g
+ + +
± −
31.0 21–55 37.0 0+ 3.0 0+ Y 0+ +
1.0
3–15
ZAMj 2–6
stalkerk
Retrotransposons
49.1 61.3 63.7 68.6 100.0 80–127
rooi B104
+
5.7 7.0
16.6 16.9 22.7 22.7 24.2 31.1
297h
+
+
+
3–13 6–16
tirantl
5.0
20.8
bloodm 15–35
+
+ + +
+
2–3
burdocko∗
auroran 15–25
3S18p Bell
1.0
11.0
HMS-q Beagle
+
+
16–32
micropiar
a Potter et al. (1979); Strobel, Dunsmuir and Rubin, (1979); Brookfield, Montgomery and Langley (1984); Yamaguchi et al. (1987); Bi´emont and Gautier (1988); Leibovitch et al. (1992); Bi´emont et al. (1994a); Charlesworth, Jarne and Assimacopoulos (1994); Csink and McDonald (1995); Furman, Rodin and Kozhemiakina (1995); Nuzhdin (1995); Vieira and Bi´emont (1996b); Cizeron et al. (1998); Hey and Eanes (unpublished results); Jordan and McDonald (1998). b Belyaeva, Ananiev and Gvozdev (1984); Bucheton et al. (1984); Bi´emont (1986); Bi´emont and Aouar (1987); Bi´emont and Gautier (1988); Leibovitch et al. (1992); Bi´emont et al. (1994a); Charlesworth, Jarne and Assimacopoulos (1994); Furman, Rodin and Kozhemiakina (1995); Nuzhdin (1995); Vieira et Bi´emont (1996b); Hey and Eanes (unpublished results). c Belyaeva, Ananiev and Gvozdev (1984); Leibovitch et al. (1992); Bi´emont et al. (1994a); Nuzhdin (1995); Hey and Eanes (unpublished results). d Potter et al. (1979); Strobel, Dunsmuir and Rubin, (1979); Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Montgomery, Charlesworth and Langley (1987); Charlesworth, Lapid and Canada (1992a,b); Charlesworth, Jarne and Assimacopoulos (1994); Aulard et al. (1995); Furman, Rodin and Kozhemiakina (1995); Vieira and Bi´emont (1996b); Cizeron et al. (1998); Hey and Eanes (unpublished results). e Peronnet et al. (1986); Montchamp-Moreau et al. (1993); Charlesworth, Jarne and Assimacopoulos (1994). f Leibovitch et al. (1992); Bi´emont et al. (1994a); Furman, Rodin and Kozhemiakina (1995); Vieira et Bi´emont (1996b); P´elisson et al. (1997); Hey and Eanes (unpublished results). g Dowsett and Young (1982); Charlesworth, Jarne and Assimacopoulos (1994). h Potter et al. (1979); Strobel, Dunsmuir and Rubin, (1979); Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Montgomery, Charlesworth and Langley (1987); Yamaguchi et al. (1987); Charlesworth, Jarne and Assimacopoulos (1994); Nuzhdin (1995); Hey and Eanes (unpublished results). i Scherer et al. (1982); Brookfield, Montgomery and Langley (1984); Montgomery, Charlesworth and Langley (1987); Charlesworth, Lapid and Canada (1992a,b); Charlesworth, Jarne and Assimacopoulos (1994); Furman, Rodin and Kozhemiakina (1995); Nuzhdin (1995); Hey and Eanes (unpublished results). j Baldrich et al. (1997); Leblanc et al. (1997). k Georgiev et al. (1990). l Molto et al. (1996); Viggiano et al. (1997). m Lavorgna et al. (1989); Costas, Valade and Naveiro (1997); Hey and Eanes (unpublished results). n Shevelyov (1993). o Gerasimova et al. (1990); Ponomarenko et al. (1997). p Bell et al. (1995); Goldberg et al. (1983). q Hey and Eanes (unpublished results). r Lankenau (1993). ∗ the copy numbers of these transposable elements were determined only on the X chromosomes. For comparison with the other elements the published numbers of insertion sites were multiplied by five to estimate the total copy number per genome. + and −: presence and absence of the element, respectively, as determined by Southern blots. w: weak labelling on the chromocenter, 0: absence of in situ labelling on the polytene chromosomes. Y: presence of the element on the Y chromosome. The values correspond to the number of insertion sites determined by different authors using in situ hybridization on polytene chromosomes; when many values obtained on different samples were available, only the minimum and maximum insertion site numbers observed are given. The absence of any numbers or symbols indicates data were not available.
10.8 11.3 14.6 17.8 18.0 20.8 20.9 23.0 24.0 25.3
copiaa
melanogaster
Species
Table 1. Distribution of transposable elements in species of the melanogaster species subgroup: the retrotransposons
45
+
+ + + + + +
mauritiana sechellia yakuba teissieri erecta orena
5.0
41.3
Fd
9.9 20–30
20–25
doce
0− − 0− 0 0 0
0−
14.7 18.6 23.8 28.4 31.3 31.5 32.3 38.7 41.0
Pf
15–20 25.0 + + 0+ ±
16.0 25–30
19.7 2.7 25–30 26.3 28.5 30–50
hobog
20–30 2.0 4.0 10.0 0 0
0–10.0
0
3–11
2–29
bari-1i
Transposons marinerh
−
−
−
+
pogoj 24-91
Sk
3.0
15.4 17.3
opusl
10.0 12.0 12.0 5–7
18.0 22.0
17–30 19.0
F Bm
Foldback
Montgomery and Langley (1984); Scavarda and Hartl (1984); Lansman et al. (1985); Ronsseray and Anxolab´eh`ere (1986); Anxolab´eh`ere and Periquet (1987); Yamaguchi et al. (1987); Bi´emont and Gautier (1988); Eanes et al. (1988); Ronsseray, Lehmann and Anxolab´eh`ere (1989); Montchamp-Moreau (1990); Shrimpton, Mackay and Brown (1990); Paricio et al. (1991); Miller et al. (1992); Bi´emont et al. (1994a); Clark, Maddison and Kidwell (1994); Hagemann, Miller and Pinsker (1994); Zabalou, Alahiotis and Yannopoulos (1994); Clark et al. (1995); Hagemann, Haring and Pinsker (1996); Paricio et al. (1996); Hey and Eanes (unpublished results). g Bingham, Kidwell and Rubin (1982); Bi´emont, Gautier and Heizmann (1988); Boussy and Daniels (1991); Periquet et al. (1994); Zabalou, Alahiotis and Yannopoulos (1994); Hey and Eanes (unpublished results). h Capy et al. (1991); Maruyama and Hartl (1991); Capy, David and Hartl (1992). i Caggese et al. (1995); Terrinoni et al. (1997); Caizzi, Caggese and Pimpinelli (1993); Dimitri et al. (1997); Moschetti et al. (1998). j Tudor et al. (1992); Boussy et al. (1993). k Merriman et al. (1995). l Charlesworth, Jarne and Assimacopoulos (1994); Hey and Eanes (unpublished results). m Silber et al. (1989); Hey and Eanes (unpublished results). For the meaning of +, −, 0, w, see legend of Table 1.
a Bucheton et al. (1984); Bi´emont (1986); Bucheton et al. (1986); Bi´emont and Gautier (1988); Ronsseray and Anxolab´eh`ere (1986); Ronsseray, Lehmann and Anxolab´eh`ere (1989); Nuzhdin (1995); Hey and Eanes (unpublished results). b Jakubczak et al. (1992); Lathe III et al. (1995). c Mizrokhi and Mazo (1990); Charlesworth, Jarne and Assimacopoulos (1994); Hey and Eanes (unpublished results). d Stacey et al. (1986); Hey and Eanes (unpublished results). e Pasyukova and Nuzhdin (1993); Vaury et al. (1994); Nuzhdin (1995). f Furman, Rodin and Kozhemiakina (1995); Brookfield,
+ + + +
6.0
8.4 13.0
35.7 36.2
+
simulans
jockeyc
R1/R2b
Non-LTR retrotransposons
10–15 15.5 16.0 17.5 21.0 30.0 30.9
Ia
melanogaster
Species
Table 2. Distribution of transposable elements in species of the melanogaster species subgroup: the non-LTR retrotransposons, the transposons and foldback elements
46
47 Table 3. Average insertion site numbers of 17 transposable elements in D. melanogaster and D. simulans, and the ratio between them. From data on Tables 1 and 2 Elements
Species D. melanogaster D. simulans
Ratio
copia mdg1 mdg3 412 1731 gypsy 17.6 297 roo/B104 I jockey F doc hobo bari-1 opus FB
18.7 21.1 10.8 24.3 4.5 1.7 12.5 22.4 78.5 19.5 36.0 41.3 22.5 29.0 6.8 16.4 22.0
7.2 4.1 3.6 2.0 1.8 1.0 0.4 3.5 2.2 1.8 6.0 8.3 1.1 1.2 1.2 5.5 1.1
ence of population size on the TE copy number (Capy, David & Hartl, 1992; Hey & Kliman, 1993). The copy number of most TEs is lower in the other five species of the melanogaster subgroup, except for hobo, mariner and FB, which have high copy numbers in D. mauritiana, D. sechellia (species of the D. simulans clade) and D. yakuba (P and pogo are absent from these species). Although many TEs are detected in D. teissieri, D. erecta and D. orena, they are present only in the chromocentric regions, with no sites over the chromosome arms (Silber et al., 1989; Capy, David & Hartl, 1992; Brunet et al., 1994; Cizeron et al., 1998). We yet do not know whether this chromocentric localization is a characteristic of these species for many TEs, or is only a characteristic of sequences homologous to the elements of D. melanogaster used as probes. TEs more specific to these species remain to be found to get a more general picture of their distribution. Note that the high copy numbers for most TEs observed in D. melanogaster could reflect the fact that many TEs were discovered in this species mainly because of their activity and capacity of causing mutation, and because of their high numbers per genome, at least in some lines, making them more easily detectable. New TEs detected by the sequencing of the D. melanogaster genome in the near future and thus not revealed by their mutator effects should provide a
2.6 5.2 3.0 12.3 2.5 1.7 35.5 6.4 36.0 10.7 6.0 5.0 20.0 23.7 5.6 3.0 20.0
less-biased sample with respect to activity, although the melanogaster-bias will still remain.
Overall distribution of TEs in species We do not have a complete estimation of copy number of TEs in all the species because sometimes only data on presence/absence are available. From the data gathered in Tables 1 and 2 and Tables 4–13, it appears that many elements are detected in many species of the genus Drosophila, but great differences exist among the TEs. For example, copia, 412 and gypsy are detected in almost all species, mainly in chromocentric regions, but with only few copies if any on the chromosome arms in most species, whereas LOA and uhu are restricted to Hawaiian Drosophila and have high insertion site numbers on the chromosome arms. Some elements can insert at many sites in the genome, as seen in D. melanogaster and D. simulans for copia and 412, while the R1Dm and R2Dm retroposons insert only at specific sites within the 28S subunit rRNA gene (Jakubczak et al., 1992; Lathe III et al., 1995), and the G element is concentrated in the nontranscribed spacer DNA of ribosomal gene clusters (Di Nocera, Contursi & Minchiotti, 1994). Some elements have a very limited distribution among the Drosophila
48 Table 4. Distribution of transposable elements in species of the Drosophila genus, Sophophora subgenus, Melanogaster group: the retrotransposons Subgroups
ananassae
montium
elegans takahashii eugracilis ficusphila suzukii
Species
ananassae malerkotliana bipectinata ercepeae merina vallismaia auraria birchii bocqueti chauvacae davidi dossoui greeni jambulina kikkawai malagassya nagarholensis nikananu seguyi serrata tsacasi vulcana elegans takahashii eugracilis ficusphila lucipennis biarmipes mimetica rajasekari
Retrotransposons copiaa
412b
0+ 0w 0+ 0+ 1 0+
1–3 0+ 0+ 0+ 0+ 0+
1731c
gypsyd
297e
ZAMf
tirantg
micropiah
+
w
+
−
+
w
− + 0+ 0+ 0+ 0+ 0+ 3 1–2 0+ 0+ 0
0+ 0+ 0+ 1 2–3 0+ 1 0+ 0+ 0+
0
0+ 0+ 0+
0w 0+ ± − + + 0
0+ 0+ 0+
−
16
+
+
−
− − −
10 14
+ + + + +
−
+ −
+ −
0+ + +
a Martin, Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino, Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan et al. (unpublished data). b Martin,
Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998). c Montchamp-Moreau et al. (1993). d Stacey et al. (1986); Marin and Fontdevila (1995, 1996). e Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984). f Baldrich et al. (1997). g Molto et al. (1996). h Lankenau (1993). For the meaning of +, −, 0, w, see legend of Table 1.
species. For instance, hobo sequences are limited to the melanogaster and montium subgroups (Daniels, Chovnick & Boussy, 1990; Simmons, 1992); the 297 element is present only in a few species of the Melanogaster group, with a weak signal in a few other species (de Frutos, Peterson & Kidwell, 1992); the I retroposon is restricted to the melanogaster subgroup (de Frutos, Peterson & Kidwell, 1992), and pogo is detected only in D. melanogaster, which is the smal-
lest species range reported among the Drosophila TEs (Boussy et al., 1993). The elements P and mariner have patchy distributions, with presence of the elements only in some species groups, with no complete relationships with the host phylogeny. Elements like copia and gypsy are less and less detected in species phylogenetically farther removed from D. melanogaster. This may be because the TE probes used are from D. melanogaster and so the dis-
49 Table 5. Distribution of transposable elements in species of the Drosophila genus, subgenus Sophophora, Melanogaster group: the non-LTR retrotransposons, transposons and foldback elements Subgroups
ananassae
montium
Species
ananassae atripex monieri ochrogaster malerkotliana bipectinata parabipectinata pseudoananassae ercepeae vallismaia varians nsp madagascar auraria baimaii bakoue barbarae biauraria bicornuta birchii bocqueti burlai chauvacae davidi diplancatha dossoui greeni jambulina kanapiae khaoyana kikkawai lacteicornis leontia lini malagassya mayri nikananu orosa parvala pennae punjabiensis quadraria rufa seguyi serrata triauraria tsacasi vouidibio vulcana
Non-LTR retrotransponsons aI
b R1/R2
+
+
c jockey
+
Transposons
Foldback
dF
eP
f hobo
g mariner
h bari-1
i pogo
+
0− 0
−
+
+
0 ± − −
− − − −
− + + + + + + + + +
−
−
jF B
+
+ +
+ −
− +
+ − + − − 0 0
+ + +
+
−
−
+
+ + +
+ −
+
− − + 0w− +
+ − + + −
−
+
+ − − − − + + + + −
+ +
+
80 + +
+
+ − + − − −
+
+ + − − + +
+
0+
+
+ + − + + + + + − + +
+
+ + + ± + − −
+ +
+
50 Table 5. Continued Subgroups
Species
Non-LTR retrotransponsons aI
elegans takahashii
eugracilis ficusphila suzukii
elegans lutescens paralutea prostipennis pseudotakahashii takahashii trilutea eugracilis ficusphila lucipennis biarmipes mimetica pulchrella rajasekari
b R1/R2
c jockey
+
− + +
+
Transposons
Foldback
dF
eP
f hobo
g mariner
h bari-1
+
0− − − − − ± −
− − − − − −
− ± − − ± −
w +
0− 0+ w+
− − −
−
+ + −
− − −
−
+
−
+ + +
+ + + +
i pogo
jF B
+
8
w −
0
+
a Bucheton et al. (1986); Stacey et al. (1986). b Jakubczak et al. (1992); Lathe III et al. (1995). c Mizrokhi and Mazo (1990). d Stacey et al. (1986). e Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). f Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990); g Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). h Moschetti et al. (1998). i Tudor et al. (1992); Boussy et al. (1993). j Silber et al. (1989). For the meaning of +, −, 0, w, see legend of Table 1.
tributions observed may in part reflect the divergence between elements in the species analyzed and those in D. melanogaster. This explanation is less evident when elements still transpose because selection for the ability to transpose may have conserved some useful sequences, as observed with the reverse transcriptase domain of retroelements which is highly conserved (McAllister & Werren, 1997). It is thus of importance to use probes from TEs specific to the species and not only probes coming from D. melanogaster, especially in species with a high content of middle dispersed repetitive DNA (Marin & Fontdevila, 1996), or whose specific TE sequences do not hybridize with D. melanogaster DNA, as for example the elements studied in D. algonquin (Hey, 1989). Note that the use of probes specific to the species under investigation leads to the detection of multiple euchromatic sites, as is observed with gandalf and copia in D. koepfera (Marin & Fontdevila, 1995, 1996), trim in D. miranda (Steinemann & Steinemann, 1991), bilbo in D. subobscura (Blesa and Martinez-Sebastian, 1997), ulysses in D. virilis (Scheinker et al., 1990), and LOA and uhu in the Hawaiian Drosophila (Table 11). This illustrates again the idea that the high copy number of TEs observed in D. melanogaster may be due in part to their high activity in this species and their detection favored by the mutations they produce.
The distribution of the above elements LOA and uhu seems to be related to the time of appearance of the species from the different islands of Hawaii (Wisotzkey, Felger & Hunt, 1997; Brezinsky, Humphreys & Hunt, 1992), making the colonization process of real importance for these elements. Why then are only some elements mobilised? Where do these elements come from? How do these elements behave in other phylogenetically distant species? These are many questions whose answers are greatly in need. The presence of elements in some lineages and their absence in others are often used to make inference about the phylogenetic behavior of these elements. Hence, copia and 412, which are found in many species of all the major Drosophila radiations, probably originated early in the history of the family (Potter et al., 1979; Martin, Wiernasz & Schedl, 1983; Cizeron et al., 1998). Moreover, since 412 is present in the chromocenter of most species and copia is absent from many species, the 412 element is thus supposed to have been present in ancestors of the Drosophila species while copia appeared more recently. These two elements have thus different evolutionary histories and behave independently, but the conservation of the sequences homologous to these elements is consistent with the Drosophila phylogeny and supports vertical transmission (Francino, Cabre & Fontdevila,
fima emarginata
sturtevanti
saltans
elliptica
cordata
emarginata
cordata neocordata elliptica emarginata neoelliptica austrosaltans lusaltans prosaltans saltans subsaltans milleri sturtevanti
bocainensis capricorni fumipennis nebulosa succinea equinoxalis insularis paulistorum pavlovskiana tropicalis willistoni
Species
+
± 0+ w
+
w +
0+ ±
0+
w
− − +
w +
+
w +
0+
+ 0+ ±
+
+
+ w + w w w
+
0+
c gypsy
b 412
+
+ + 0± + +
a copia
− −
−
−
−
d 297
Retrotransposons
−
−
e tirant
+
+
f micropia
−
±
− −
−
− − − −
− −
−
− − −
− −
gI
−
−
−
−
h jockey
+
+
+
+
+
+
iF
Non-LTR retrotransposons
−
− − + + + + + + +
− −
+ + 0+ + + + 1 + + +
jP
− −
− − − − − −
−
− − − − − − − − − −
k hobo
− +
−
−
−
−
−
+
+ +
+
+
+
+ +
+
+ w +
+
m bari-1
Transposons l mariner
−
n pogo
(1992); Boussy et al. (1993). For the meaning of +, −, 0, w, see legend of Table 1.
a Martin, Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino, Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan and McDonald (1998). b Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998). c Stacey et al. (1986); Marin and Fontdevila (1995, 1996). d Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984). e Molto et al. (1996). f Lankenau (1993). g Bucheton et al. (1986); Stacey et al. (1986). h Mizrokhi and Mazo (1990). i Stacey et al. (1986). j Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). k Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). l Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). m Moschetti et al. (1998). n Tudor et al.
Saltans
bocainensis
Willistoni
willistoni
Subgroups
Groups
Table 6. Distribution of transposable elements in species of the Drosophila genus: Willistoni and Saltans groups
51
52 Table 7. Distribution of transposable elements in species of the obscura, pseudoobscura and affinis subgroups of the Obscura group: the retrotransposons Subgroup
obscura
pseudoobscura
affinis
Species
Retrotransposons a copia
b mdg-1
c mdg-3
d 412
bifasciata guanche madeirensis microlabis obscura subobscura subsilvestris tristis
+ − 0+ 0w 0+ ± +
+ +
− −
+ +
+ + + +
+ − + +
1–2 0+ 3–8 0+ 2–10 1–4 +
miranda persimilis pseudoobscura pseudo bg
+
+ + +
+ + + +
+ + 0–1+ +
+ + + +
− − − −
+ + −
+ + + +
+ + + + +
+ + + + +
0+ + + + +
+ + + + +
− − − − −
+
− − − − −
affinis algonquin azteca narragansett tolteca
0–30+ + 0w + + +
e 1731
f gypsy
+ + + +
16
g gypsyDs
4–7
h 297
i tirant
j 3S18
− −
−
− −
− − −
+
− − − −
a Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); de Frutos, Peterson and Kidwell (1992); Francino, Cabre and Fontdevila (1994); Jordan and McDonald (1998). b de Frutos, Peterson and Kidwell (1992). c de Frutos, Peterson and Kidwell (1992). d Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); de Frutos, Peterson and Kidwell (1992); Cizeron et al. (1998). e Montchamp-Moreau et al. (1993). f de Frutos, Peterson and Kidwell (1992); Stacey et al. (1986). g Alberola and de Frutos (1993). h Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); de Frutos, Peterson and Kidwell (1992). i Molto et al. (1996). j Bell et al. (1995); Goldberg et al. (1983). For the meaning of +, −, 0, w, see legend of Table 1.
1994; Csink & McDonald, 1995). Since the Obscura group species do not have the element 297 (Table 7), this element may have appeared after the divergence of the Melanogaster and Obscura groups; the I element, which is restricted to the melanogaster subgroup, arose before the radiation of species within the Melanogaster species group but after the separation of the Sophophora species groups; the pogo element appears only in D. melanogaster (Boussy et al., 1993), suggesting a recent origin. Such results have lead to various interpretations but the horizontal transfer hypothesis is still the preferred mechanism proposed (Clark & Kidwell, 1997). Horizontal transmission events are thus well supported for the transposons P (Clark, Maddison & Kidwell, 1994; Hagemann, Haring & Pinsker, 1996) and mariner (Maruyama & Hartl, 1991), and are suggested for hobo (Daniels, Chovnick & Boussy, 1990; Simmons, 1992), pogo (Boussy et al., 1993), the retroposons I (Bucheton et al., 1986, 1992) and jockey (Mizrokhi & Mazo, 1990), and the retrovirus gypsy (Stacey et al., 1986; Alberola & de Frutos, 1993).
The alternatives to horizontal transfers include stochastic losses, variation in evolution rates, presence of highly conserved sequences, and ancestral polymorphism (Cummings, 1994; McAllister & Werren, 1997; see Capy, Anxolabéhère & Langin, 1994; Clark, Maddison & Kidwell, 1994, for a discussion). Ancestral polymorphism with differential rates of loss and evolution of elements between species lineages, and the presence in the genome of multiple divergent subfamilies of the same family of TEs, as observed for P and mariner (Clark et al., 1995) and R1 and R2 elements (Burke et al., 1998), could explain the fact that some TE-trees do not match the species phylogeny (Clark, Maddison & Kidwell, 1994; Nouaud & Anxolabéhère, 1997). The presence of specific elements in a species or a group of species raises thus the question of the recent formation of these TEs. Recombination and rearrangements between ancient inactive sequences, as proposed for the 297 sequence (Martin, Wiernasz & Schedl, 1983) and the I element (Bucheton et al., 1992; Dimitri et al., 1997), or recombination between different TEs, as for the micropia
ambigua bifasciata guanche madeirensis microlabis obscura subobscura subsilvestris tristis helvetica miranda persimilis pseudoobscura pseudo bg affinis algonquin athabasca azteca narragansett tolteca
obscura
pseudoobscura
affinis
± + + + + +
+ + + +
± + +
+ +
aI
+ + +
− −
+
+ + + + +
− − −
+ + + +
+ +
+
+
dF
− −
− − − −
− − − −
c Jockey
− − −
− −
− − − −
− − − −
− −
eG
26–33
f bilbo
Non-LTR retrotransposons b R1
+
25
g trim
+ + +
+ +
+ + + + +
+ + + +
+ 1+ + +
hP
2
+
+
i T-type
− − − − − −
− − − −
− − − −
− − −
+
± −
− − ±
+ + + +
± ±
k mariner
Transposons j hobo
+ + +
+ +
+ + +
+ +
l bari-1
−
−
m pogo
− − −
0
n FB
Foldback
al. (1989). For the meaning of +, −, 0, w, see legend of Table 1.
a de Frutos, Peterson and Kidwell (1992); Bucheton et al. (1984). b Jakubczak et al. (1992); Lathe III et al. (1995). c Mizrokhi and Mazo (1990); de Frutos, Peterson and Kidwell (1992). d de Frutos, Peterson and Kidwell (1992). e de Frutos, Peterson and Kidwell (1992). f Blesa and Martinez-Sebastian (1997). g Steinemann and Steinemann (1991). h Brookfield, Montgomery and Langley (1984); Anxolab´eh`ere, Nouaud and Periquet (1985); Anxolab´eh`ere and Periquet (1987); de Frutos, Peterson and Kidwell (1992); Garcia-Planells et al. (1998); Hagemann, Miller and Pinsker (1992); Miller et al. (1992, 1995); Paricio et al. (1991, 1996). i Hagemann, Haring and Pinsker, (1996). j Daniels, Chovnick and Boussy (1990). k Capy, David and Hartl (1992); Brunet et al. (1994). l Moschetti et al. (1998). m Tudor et al. (1992); Boussy et al. (1993). n Silber et
Species
Subgroup
Table 8. Distribution of transposable elements in species of the obscura, pseudoobscura and affinis subgroups of the Obscura group: the non-LTR retrotransposons, transposons and foldback elements
53
Subgroups
ellisoni eohydei hydei neohydei mercatorum mercatorum paranaensis mulleri aldrichi arizonae arizonensis borborema buzzatii huaylasi hydeoides koepfera mayaguana martensis meridiana mojavensis mulleri navojoa nigrodumosa peninsularis richardsoni serido stalkeri starmeri straube uniseta venezolana wheeleri repleta melanopalpa meridiana neorepleta repleta
fasciola hydei
Retrotransposons
Non-LTR retrotransposons
+
0−
0+
+ +
+ + +
+ +
−
0−
+ +
+
+
+
+ +
− +
0w
+
±
+
0w− +
− −
−
−
−
+
0+
−
+
+
−
+ 11–15
+
−
−
−
0–30
0–5
− + +
−
− +
+
−
+ 11 + + +
−
+
−
−
−
+
− +
−
−
−
+
+
+
+
+
a copia b 412 c gypsy d 297 e ZAM f ulysses g tirant h penelope i telemac j micropia k I l R1/R2 m jockey n F
− littoralis lummei − montana novomexicana texana virilis −
Species
0
−
−
− −
−
−
Transposons
−
− −
−
−
±
− −
−
−
− − −
−
±
± − −
+
+
+ w+ +
+
+
+ +
+ w
+
+ + + +
+ + + + + + + +
+ − +
+ + + + 5–10 + +
+ +
+
+
p hobo marinerq bari-1r gandalfs
0− −
−
−
oP
c Stacey et al. (1986); Marin and Fontdevila (1995, 1996). d Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984). e Baldrich et al. (1997). f Scheinker et al. (1990). g Molto et al. (1996). h Petrov et al. (1995); Evgen’ev et al. (1997). i Vieira et al. (1998). j Lankenau (1993). k Bucheton et al. (1986); Stacey et al. (1986). l Jakubczak et al. (1992); Lathe III et al. (1995). m Mizrokhi and Mazo (1990). n Stacey et al. (1986). o Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). p Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). q Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). r Moschetti et al. (1998). s Marin and Fontdevila (1995). For the meaning of +, −, 0, w, see legend of Table 1.
data); Jordan and McDonald (1998). b Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998).
a Martin, Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino, Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan et al. (unpublished
Repleta
Subgenus Drosophila Virilis virilis
Groups
Table 9. Distribution of transposable elements in species of the Drosophila genus, subgenus Drosophila, Virilis and Repleta groups
54
+ +
−
−
hypocausta 0w neohypocausta pararubida rubida immigrans formosana immigrans signata lineosa lineosa nasuta albomicans kepulauana kohkoa nasuta + pulaua sulfurigaster tongpua quadrilineata quadrilineata 0+
hypocausta
Retrotransposons
1
0+
−
−
−
+ +
+
+
− −
+
−
+
−
−
− −
−
−
a copia b 412 c gypsy d 297 e tirant f micropia g I
+ +
−
+
+
h R1/R2 i jockey j F
62
Transposon
−
±
−
±
−
− − −
−
−
− w
w w
+
+ w
− +
−
123
m hobo n mariner o bari-1 p pogo q uhu
0− − − − − − − − − − − − − − ± − − −
− −
−
−
k LOA l P
Non-LTR retrotransposons
Wisotzkey, Felger and Hunt (1997). For the meaning of +, −, 0, w, see legend of Table 1.
a Martin, Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino, Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan et al. (unpublished data); Jordan and McDonald (1998). b Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998). c Stacey et al. (1986); Marin and Fontdevila (1995, 1996). d Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984). e Molto et al. (1996); f Lankenau (1993). g Bucheton et al. (1986); Stacey et al. (1986). h Jakubczak et al. (1992); Lathe III et al. (1995). i Mizrokhi and Mazo (1990). j Stacey et al. (1986). k Wisotzkey, Felger and Hunt (1997). l Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). m Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). n Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). o Moschetti et al. (1998). p Tudor et al. (1992); Boussy et al. (1993). q Hunt, Bishop and Carson (1984); Brezinsky, Humphreys and Hunt (1992);
Immigrans
pavani pinicola
euronotus melanica
Mesophragmatica pavani Pinicola pinicola
melanica
Melanica
lacertosa robusta sordidula
neotestecea putrida
robusta
Robusta
Species
Testecea
Subgroups
Groups
Table 10. Distribution of transposable elements in species of the Drosophila genus, subgenus Drosophila, other groups
55
56 Table 11. Distribution of transposable elements in species of the Drosophila genus, Hawaiian Drosophila group Subgroups
planitibia
Species
differens hawaiiensis heteroneura neutralis picticornis planitibia puralua silvestris
adiastola
adiastola ornata peniculipedis setosimentum
grimshaw mimica antopocerus fungus feeders cardini
grimshawi mimica
guarani pallidipennis tripunctata quinaria
Retrotransposons
Non-LTR retrotransposons
a copia
b 412
c LOA
−
−
Transposons dP
e hobo
f mariner
47
g uhu
58 1–16(−) − −
40
166 23 117
36 −
130 0 0 0 0 −
±
−
−
nigra arawakana cardini dunni neocardini
− − −
−
guaramunu pallidipennis unipunctata limbata
− − − +
−
96 51 122 153
− −
+ 60 + 0
−
−
a Martin, Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino,
Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan et al. (unpublished data); Jordan and McDonald (1998). b Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998). c Wisotzkey, Felger and Hunt (1997). d Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). e Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). f Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). g Hunt, Bishop and Carson (1984); Brezinsky, Humphreys and Hunt (1992); Wisotzkey, Felger and Hunt (1997). For the meaning of +, −, 0, w, see legend of Table 1.
element (Lankenau, 1993), may be involved in such appearance of new TEs in a species.
Concluding remarks While species may have quickly diverged according to the element subfamilies that invaded their genome, the fate of these elements in various populations of the species may considerably vary. Indeed, events in which one element is suddenly mobilized and invades the chromosomes have been reported for elements as
diverse as copia, gypsy, P and doc (Biémont, 1992). Although this has been observed in laboratory lines, and some of these lines have specific host genes controlling the element (Pélisson et al., 1997), it has also been reported in natural populations, as for the mdg3 and 412 elements (Biémont et al., 1994b; Vieira & Biémont, 1996a). Why then are most populations not invaded by these elements? In particular, why is gypsy still maintained in very low copy number (1–2 copies in average per individual) with a high polymorphism of insertion between individuals, in natural populations of D. melanogaster and D. simulans, while it has
funebris macrospina multispina subfunebris aracatacas gibberosa talamancana melanica polychaeta repletoides canalinea camargoi gaucha
Funebris
Annulimana
Melanica Polychaeta Tumiditarsus Canalinea Dreyfusi
0
a copia
0w
b 412
d tirant
−
c ulysses
−
Retrotransposons
+
e micropia
−
fI
+
g jockey
Non-LTR retrotransposons
w
+
w
k bari-1
− − − − − −
±
j mariner
w −
−
i hobo
− − −
− − − −
hP
Transposons
−
l pogo
Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). i Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). j Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). k Moschetti et al. (1998). l Tudor et al. (1992); Boussy et al. (1993). For the meaning of +, −, 0, w, see legend of Table 1.
a Cizeron et al. (unpublished results); Jordan et al. (unpublished data); Jordan and McDonald (1998). b Cizeron et al. (1998). c Scheinker et al. (1990). d Molto et al. (1996). e Lankenau (1993). f Bucheton et al. (1986); Stacey et al. (1986). g Mizrokhi and Mazo (1990). h Brookfield, Montgomery and Langley (1984);
Species
Groups
Table 12. Distribution of transposable elements in species of various groups of the Drosophila genus
57
58 Table 13. Distribution of transposable elements in species of the subgenus Hirtodrosophila and the genus Zaprionus Species
Retrotransposons
Transposons
a copia
b 412
c 297
Subgenus duncani
Hirtodrosophila w
+
−
Genus tuberculatus vittiger indianus inermis spinipilus ornatus sepsoides mascariensis
Zaprionus 0+ +
1–2 +
−
dP
e hobo
f mariner
−
−
+ + +
− + + − −
a Martin,
Wiernasz and Schedl (1983); Stacey et al. (1986); Brookfield, Montgomery and Langley (1984); Francino, Cabre and Fontdevila (1994); Cizeron et al. (unpublished results); Jordan et al. (unpublished data); Jordan and McDonald (1998). b Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984); Stacey et al. (1986); Francino, Cabre and Fontdevila (1993); Cizeron et al. (1998). c Martin, Wiernasz and Schedl (1983); Brookfield, Montgomery and Langley (1984). d Brookfield, Montgomery and Langley (1984); Daniels and Strausbaugh (1986); Stacey et al. (1986); Anxolab´eh`ere and Periquet (1987); Lansman et al. (1987); Clark et al. (1995); Regner et al. (1996); Clark and Kidwell (1997). e Daniels and Strausbaugh (1986); Daniels, Chovnick and Boussy (1990). f Zelentsova et al. (1986); Capy, David and Hartl (1992); Brunet et al. (1994). For the meaning of +, −, 0, w, see legend of Table 1.
the potential to invade the genome at least under some specific permissive genomic conditions (Bucheton et al., 1992)? It may be that such an event is rare in natural populations and that the individuals in which it happens are eliminated before being capable of transmitting their chromosomes. Position effect may also be important in such processes, such that an insertion, even an active sequence, may be inactivated by its close genomic environment. However, when an active sequence gets to an adequate site, it has a good possibility of invading the genome as long as this genome has not already established conditions repressing the activity of the element. An element transmitted to a new organism by horizontal transfer may thus quickly invade the genome since no repression is at work, as illustrated by D. hydei, which has a strong transcriptional activator of copia but has no copia elements (Cavarec, Jensen & Heidmann, 1994). The same process may happen with new mutated elements or with elements from diverse subfamilies as is demonstrated for P and mariner elements and more recently for the non-LTR element HeT-A found only
in telomeric regions (Danilevskaya, Lowenhaupt & Pardue, 1998). It could be that many retrotransposable elements will present sequence polymorphism as soon as we look for it, as found for the retrotransposon Tnt1 in tobacco (Casacuberta, Vernhettes & Grandbastien, 1995; Vernhettes, Grandbastien & Casacuberta, 1998) and for viral quasispecies (Domingo & Holland, 1994). If so, these elements might represent cases of the master copy process found with LINE and Alu elements in humans (Quentin, 1988) associated with presence of multilineages within a single species (Cummings, 1994). Hence, although it is accepted that a recent invasion of a TE in a natural population may lead to a rapid change in mutation rate (Mukai et al., 1985), we still need to understand its true impact on population variability and local adaptation. Only when more details of factors influencing the genomic dynamics of many TEs in various organisms are known can new models of their population genetics in natural populations be established and their behavior during the course of evolutionary processes better assessed.
59 Acknowledgements We thank C. Arnault, I.A. Boussy, C. Vieira, and the two referees for useful comments, J. Hey and W. Eanes, I.K. Jordan and J.F. McDonald, for their unpublished data. This work was supported by the Centre National de la Recherche Scientifique (UMR 5558), the Ministère de la Recherche, the Bureau des Ressources Génétiques, the génome programme of the CNRS.
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