Heredity 73 (1994) 377—385 Received 10 February 1994 The Genetical Society of Great Britain

The mariner transposable element in the family

FREDERIC BRUNET, FABIENNE GODIN, JEAN A. DAVID & PIERRE CAPY* Laboratoire Populations, Genétique et Evolution, CNRS, 91198 Gif/Yvette Cedex, France

Thedistribution of the mariner transposable element among Drosophilidae was investi- gated using three differetìt techniques, i.e. squash blots, Southern blots and PCR amplification, using two sets of primers (one corresponding to the Inverted Terminal Repeats and the other to two conserved regions of the putative transposase). Our results and those of others show that the distribution of mariner is not uniform and does not follow the phylogeny of the host species. An analysis of geographical distribution, based on endemic species, shows that mariner is mainly present in Asia and Africa. At least two hypotheses may be proposed to explain the specific and geographical distributions of this element. Firstly, 'they may be the results of several horizontal transmissions between species and/or between Drosophila species and one or several donor species outside the Drosophilidae family. Secondly, these particular distributions may correspond to the evolution of the mariner element from an ancestral copy which was present in the ancestor of the Drosophilidae family.

Keywords:Drosophila,mariner, transposon, phylogeny.

al., 1994). In all cases, the evolutionary history of these Introduction elements is not simple and more information is neces- Thedistribution of the mariner transposable elements sary about the variability within and between more or in Drosophila was previously investigated by less closely related species. Maruyama & Hartl (1991 a). In their analysis, species In this respect, we have investigated the Drosophili- belonging to different groups, subgenera and genera dae family to extend the previous work of Maruyama were screened, showing a distribution with a major gap & Hartl (1991a), which included 78 species. The between the melanogaster group and the number of species analysed in this family is now 127. subgenus. On the basis of this specific distribution and For several groups, we have screened almost all the of the high similarities of DNA sequences of copies available species. Moreover, three more or less sensi- extracted from different species, it was suggested that tive techniques, i.e. squash blots, Southern blots and horizontal transfers had occurred between D. mauri- PCR (polymerase chain reaction) have been used here tiana and Z. tuberculatus or between species related to while Maruyama & Harti (1991 a) only used a Southern these. blot detection. The horizontal transfer hypothesis is commonly The aim of this analysis was to obtain a better idea suggested from the analysis of transposable element of the specific and geographical (based on endemic distributions and from the comparison of their species) distributions of the mariner element. This is a sequences (Daniels et al., 1990; Mizrokhi & Mazo, first step before a detailed analysis, at the nucleotidic 1990; Lawrence etal., 1992; Robertson, 1993). On the level, of the polymorphism within and between species. other hand, several alternative hypotheses, among Our results show that some mariner-related sequences which genetic drift, existence of ancestral elements on can be detected in many Drosophila species. Moreover, which high selective constraint may act in a small part in many species, a particular class of deleted elements of the element, ancestral polymorphism, different rates seems to represent the major part of the copies. How- of evolution according to the activity level of the copies ever, in different species, different classes of deleted and according to the host species, could also explain elements exist. The geographical and specific distribu- the phylogenetic oddities of several elements (Capy et tions among species will be discussed with reference to the different hypotheses reviewed by Capy et al. *Correspondence (1994). 377 378 F.BRUNETETAL.

corresponding to the WVPHEL and YSPDLAP con- Materials and methods served regions in the putative transposase (see Robert- son, 1993; Langin et al., 1994). These particular Species primers deduced from the comparison of mos-1 (an Eighty-threespecies belonging to the Drosophilidae active mariner element of D. mauritiana, Bryan et al., family were screened. Most of them belong to the huge 1987) and MLE (an inactive mariner-like element of Drosophila . This genus is subdivided into sub- the lepidopteran Hyalophora cecropia, Lidhoim et al., genera among which two, the Sophophora and 1991), will be called the 'internal primers'. The PCR Drosophila subgenera, contain a large number of amplification was performed as follows: less than 10 ng species. These subgenera are themselves classically of DNA from regular DNA extraction or 1 1uLofa divided into groups (e.g. the melanogaster or the rough extraction following the protocol of Gloor & obscura groups) and groups containing too many Engels (1991) were used in 50 1uLofa total reaction species are subdivided into subgroups (e.g. the melano- volume containing 0.5 units of Taq polymerase gaster or the ananassae subgroups). (Promega). Amplifications were performed on the Particular attention was paid to the ananassae and Trio-Thermoblock of Biometra. Prior to the first cycle, montium subgroups belonging to the melanogaster a denaturation at 95 °C during 5 mm was performed, group, to the obscura group and to the Zaprionus then the basic cycle corresponded to a denaturation at genus. Moreover, three other genera, Chymomyza, 95 °C for 30 s, an annealing phase at 52°C for 1 mm Scaptodrosophila and Scaptomyza, were also con- and an elongation phase at 72°C for 2 mm. After the sidered. Among the 83 species here analysed, 34 were last cycle, the temperature was decreased to 4 °C. The in common with Maruyama & Harti (1991 a). total number of cycles varied between 35 and 40. To be sure that the amplified fragments were related to mariner, the gels with the PCR products were trans- Squashblots and Southern blots ferred on a nylon filter and hybridized with mariner Squashblots were performed as described by Tchen et probes of D. mauritiana as for squash blots and al. (1985). For Southern blots, DNA was extracted Southern blots. from about 20—30 using the technique of Maruyama & Hartl (1991a). Total DNA was then digested by HindIII and BamHI, two restriction Results enzymes that do not cut in the peach sequence, an Investigationswere mostly carried out on species of the inactive element described in D. mauritiana (Jacobson Sophophora subgenus of Drosophila, i.e. the ananassae et al., 1986). Gels were transferred according to the and the montium subgroups within the melanogaster Southern technique (Southern, 1975) and probed with group, the obscura group and on species of Zaprionus a mixture of pchlV and pch V probes described in with its two subgenera (Zaprionus and Anaprionus). Maruyama & Hartl(1991a). Several other species randomly sampled from the Drosphilidae family were also tested. PCRamplifications PCRamplifications were performed using two sets of Theananassae subgroup primers (Fig. 1). Firstly, the inverted repeats of the D. Twelveof the 20 species known in this subgroup have mauritiana peach element and, secondly, primers been screened. Detailed results are summarized in

internal primers TGGGTGCCACATGAGTTG ATGAGTGGTCTGGACCGGGGT

1 Fig. 1 PCR primers used for the Putative transposase M WVPHEL YSPDLAP 1 amplification of the mariner element 0 119 124 276 282 346 from total genomic DNA. The • ATG TAA • WVPHEL and YSPDLAP regions mariner element I 172 1210 1286 were determined from the comparison between the mariner-like element (MLE) of Hyalophora cecropia * (Lidholm etal., 1991) and the peach inverted repeat primers CCAGGTGTACAAGTAGG GTATGAACATGTGGACT element of D. mauritiana (Jacobson et al., 1986). MARINER ELEMENTS IN THE DROSOPHILIDAE 379

Table1 Distribution of the mariner element detected by three different techniques in the species of the ananassae Table 1. The species are distributed among the four subgroup in the melanogaster group complexes of this subgroup, i.e. the bipectinata (four species), the ananassae (four species), the ercepeae PCR (three species) and the nonclassified species (one Southern blot species) complexes. In this subgroup, only two species Species Squash blot (no. of bands) ITR NT were previously screened by Maruyama & Hartl (1991a). bipectinata complex The three techniques of detection were used for all ++ 1—2 + D. bipectinata + species.For most of them, some positive signals were D. malerkotliana ++ + 9 + + observed ++ (Fig. 2). The only exception is D. varians D. parabipectinata 10—15 + + species) for which no amplification was ++ 0 + + (nonclassified D. pseudoananassae obtainedwith internal primers. The hybridization ananassae complex signals and the numbers of bands observed by D. ananassae ++ 3-5 + + Southernblots vary greatly from one species to D. atripex ++ + 8 + + another.Assuming that, in this subgroup, the two D. monieri +/ — 7 + + restrictionendonucleases used do not cut into the + + D. ochrogaster marinercopies, our results suggest that the number of ercepeae complex copies is highly variable. Indeed, estimations of the D. ercepeae ++ + + 10-20 + + numberof copies, based on the number of bands D. vallismaia 15-20 + + observedby Southern blots, show that this number D. n.sp. Madagascar + couldvary from 1 to 2 in D. bipectinata and D. varians Ungrouped species to 10 to 20 in the species of the ercepeae complex. For D. varians + 2 + — D.monieri no signal was detected by squash blot while faint hybridizing bands were observed by Southern A blank means that the technique was not used. blot. The main difference between these two tech-

IA. 1111.00* Anaprionus subgenus I A. bogorlensis Zaprionus genus . kOIOdfl0* _____hi_sn I Z. -*2? a n.— I z. a Zaprionu; subgenus Z. vittlg.r '!4 S. Z.tubsrculatus Z. spinIpIlus S4a. ',• Z. indlanus

I D. bltssclsta s—s

0. subobscura Obscurs group D. peeudoobscura - 0. khumensls .

ficusphhla subgroup D. licusphhla -, ... Is- S...* I 0. bekouC (0*nln) esas a 0. bk0ue (Ivory Coast) Drosophila genus I I D.dsvldh montlum subgroup I 0. klkkaw& s-es- • • 0. loontla .--- Fig.2 Southern blot hybridizations. In each case, the total genomic DNA was 0. extractedfrom about 20—3 0 individ- D.ercepeas ' uals * a i using the technique described by .. subgroup I & Hart! (1991a). In the Maroyama I subgenus very faint bands D. parsblp.ctlnata Anaprionus 0. aredetected. atrtpex 380 F.BRUNETETAL. niques was that the washing stringency was generally contain a large number of copies (assuming that no higher for the former compared with the latter. restriction sites for Hindlil and BamHI exist in these Therefore, it is possible that the similarity between the copies). Such is the case for D. bakoue, D. davidi, D. mariner copies of this species and the D. mauritiana kikkawai and D. leontia in which the average number probe is lower than for the copies detected in the other of copies is about 14. All these copies were detected by species of this subgroup. Southern blots. By PCR amplification, no product was obtained for the eight species tested, using either set of primers. Therefore, the elements detected may corre- Themontium subgroup spond to deleted copies (in particular in the regions of the PCR primers). On the other hand, while these Inthis subgroup, 14 species were previously screened by Maruyama & Harti (1991a). In the present work, 18 copies are easily detectable by Southern hybridization, species were tested corresponding to 13 newly investi- it is possible that the divergence with the D. mauritiana gated species and five species already analysed. The elements is strong enough to prevent the hybridization results are given in Table 2 and some hybridizations of the PCR primers. are shown in Fig. 2. Considering the species in common, the results of Othersubgroups in the melanogaster group the two analyses are in agreement with the exception of D. serrata. Here, Maruyama & Hartl (1991 a) found a Withinthe melanogaster group, some mariner-like positive signal by Southern blot whereas we failed to elements were detected in seven out of the eight sub- groups analysed (Fig. 3). Only the elegans and find anything with the three techniques used. However, eugracilis subgroups appear to be free of such ele- because two different strains were used, it is possible that this species is polymorphic for the presence or ments. In the takahashii subgroup, some elements seem absence of the element. to be present in D. lutescens and D. pseudotakahashii With regard to the new species, the montium sub- but not in D. takahashii itself. Therefore, the mariner elements seem to be randomly distributed within and group is quite heterogeneous. Several species seem to be free of the mariner element (D.aurariafrom between the different subgroups which compose this Maruyama & Hartl (1991 a), D. burlai, D. chauvacae, D group. Moreover, the hybridization intensities vary vouidibioi and D. vulcana) whereas several others from one species to another. Such a result could be explained by different degrees of similarities with the D. mauritiana probe. In this case, it will be interesting Table 2 Distribution of the mariner element detected by to sequence several of these elements to determine three different techniques in the species of the montium their phylogenetic relationships. subgroup in the melanogaster group PCR Theobscura group Southern blot Thisgroup, which also belongs to the same Squash blot (no. of bands) ITR INT Drosophila species Sophophora subgenus, was previously investigated by — — Maruyama & Hartl (199 la). However, none of the six D. bakoue (Bénin) + + 14 — — species analysed contained any mariner copies. In the D. bakoue (Congo) + + 9 D. bakoue (Ivory Coast) + 12 — — present work, 10 species were tested, three of them D. bocqueti + / — 0 — — being in common with the previous investigation. In D. burlai — contrast with the previous results, all the species tested D. chauvacae — 0 — — seem to harbour some mariner elements (Table 3). The D.davidi ++ 16 — — main difference between the two investigations is D.dossoui ++ 4 — — probably the washing stringency of the hybridized D. greeni + + filters. Therefore, it is quite possible that the elements D. kikkawai + + / — 14 detected in this group are more divergent from those of D. leontia 16 D. mauritiana. It must be stressed, however, that some + + D. malagassya amplifications were obtained using the PCR primers D. nikananu + + + D.serrata +— 0 — — corresponding to the ITR. D. tsacasi + + — D. vouidibioi TheDrosophila, Zaprionus and other genera D. vulcana — Forthe remaining species tested belonging to the A blank means that the technique was not used. Drosophila genus, the results are summarized in Table MARINER ELEMENTS IN THE DROSOPHILIDAE 381

I ittora I is Lumnei — yinis montana viriLis : ananassae subgroup anizonensis bipectinata courtex buzzati r +D.bipectinata eohydei f+ + D.maLerkotLiaria — mojavensis +0.parabipectinata - repteta—4-- D.mercatorun L + p•pseudoananassae - D.mulLen - D. ananassae coepLex neohydei r ++ D.ananassae - D.paranaensis + 0.atripex -+' D.repL eta J. +D.unonieni ananassae p.tacertosa + P.ochrogaster - p.meLanica - robuste - ercepeae coniLex D.robusta +D. - P.sordiduLa r ercepeae • Drosophila - 4+ D.vatLismaia - D.atbomicans +D.nsp Madagascar - -+? 0. imigrans luninigrans unclassified species - +? 0.nasuta —+ 0.varians D. adiastota montiun 0. grinshawi subgroup - D.auraria Hawaiian - D. heteroneura +0.bakoue Benin - DrosophiLa - D. mimica +D.bakoue Congo 0. neutratis +P.bakoue Ivory C. P. punatua + 0.barberae — cardini— • 0. arawakana + P.bicornuta - - P.birchii - quinaria — D.Lithata - D.bocqueti - funebnis —-+? 0.funebris • D. burLai - D.chauvacae - affinis + 0. +D.davidi 0. aLgonquin + + P.diptancatha 0.azteca + - 0.dossoui + D.bifasciata montiun +0. greeni • Drosophila — +P.guanche - D.jathutina +0.kitunensis ++ D.kikkawai - obscura— +0.microLabis +D.leontia 0. miranda +D. +0.obscura maLagassya ++ P.nikaruanu D. persimitis + 0. -+ D. pennae pseudoobscura + P. quadrania +D.subobscura + D. +0.subsiLvestris seguyi +- D.serrata • Sophophora -- meLanogaster— ++ D.tsacasi - 0.vouidibioi 0. neocordata -- P.vutcana - saltans D. saLtans -+ D.sturtevanti ficusphita subgroup La +P.ficusphiLa D. capricorni ficusphi —wiLtistoni 0. nebutosa elegans subgroup f: P. pauUstorun elegans - D.eLegans -fuss +P. fima eugraci I is subgroup - - —eugracilis - 0.eugracitis Dorsitopha -I.?0.busckii suzukii subgroup + 2.vittiger + + + P.Lucipennis Z.indianus + + 0.miunetica 2.spinipiLus suzukui + P. +2.ornatus r putchretLa + D.biarmipes +Z.(cf.) yittiger takahashii subgroup ++ Z.tubencuLatus - + 0.Lutescens -- 2.sepsoIdes I I - P.paratutea - Z.mascariensis I I L takahashii - P.prostipennis -- 2.inermis j - + P.pseudotakahashli Zaprionus +2.koLodkinae - - D.takahashii ++ 2. 1 ghesquierei subgroup +2.verruca I unelanogaster Zapnionus - - P.orena +7.cercus -- D.erecta L ++ P.yakuba +A. bogoriensis ++ 0.teissieri Anapnionus +A.Lineosa -- D.meLanogaster • Chymomyza - C.bf color ++ P.simulans ++ D.maunitiana - - D.(Cf.) finitima ScaptodrosophiLa ++ 0.secheLtia - Scaptomyza — Parascaptomyza +? S.paLtida Fig. 3 Summary of the different results obtained by Maruyama & Hart! (199 la), in the left column, and in the present work, right column. +,existenceof hybridizing signal(s); —,nohybridizing signal. 382 F. BRUNET ETAL.

Table 3 Distribution of the mariner element detected by 4. Among these data we can observe the putative three different techniques in the species of the obscura group absence of mariner in D. arawakana (cardini group) and in D. limbata (quinaria group) whereas some PCR hybridization was obtained on D. fima genomic DNA Southern blot (fima group). Moreover, a few species seem to be ITRINT Drosophila species Squash blot(no. of bands) positive while they appeared negative from the Maruyama & Harti (1991 a) analysis, e.g. D. virilis and Palaeartic species D. littoralis (virilis group). D. bifasciata + 12 + + Concerning the Zaprionus genus, two species D.guanche + belonging to the Anaprionus subgenus and 13 species D. obscura + + of the Zaprionus subgenus were tested (Table 5). With D. subobscura + 5 + the exception of Z. sepsoldes, Z. mascariensis and Z. D. subsilvestris + inermis, all the species showed some hybridising bands American species with D. mauritiana probes. The signals are generally D.affinis + ++ weak in the Anaprionus subgenus but can be strong in D. azteca + the Zaprionus subgenus for almost all the positive D. pseudoobscura + 8 species. This result suggests a better identity between D. mauritiana and the species of the Zaprionus sub- African species D. kitumensis + 5 — + genus than with the two species of the Anaprionus sub- D. microlabis + genus. Concerning the species belonging to the three other A blank means that the technique was not used. genera (Chymomyza, Scaptodrosophila and Scapto- myza) no signal was detectable by Southern hybridiza- tion. However, some amplification products were Table 4 Distribution of the mariner element detected by obtained from total genomic DNA of Scaptomyza three different techniques in some species of the Drosophila pallida using the two sets of primers. genus M&H PCR Discussion SouthernSquash Detection of the elements Drosophila genus blot blot ITRINT Figure 3 summarizes all the data concerning the Sophophora subgenus distribution of the mariner element among the species saltans group of the Drosophilidae family. The data of Maruyama & D. sturtevanti — + / — Hartl (1991a) and of the present work were pooled. It fima group D.fima +++ appears that some gaps exist and that the element can Drosophila subgenus be present in a given species but absent in a closely virilis group related one. Such is the case between the species of the D. littoralis — + + + montium subgroup. Moreover, in the melanogaster D.virilis — ++ +? subgroup, our results confirm those of Maruyama & repleta group Hartl (1991a), i.e. the absence of the mariner element D. repleta — +? in D. melanogaster, D. erecta and D. orena. immigrans group — In this respect, it must be stressed that it is not D. immigrans + / — +? possible to state that a species is free of the mariner D. nasuta — +? element. For instance, in the present study the genomic funebris group DNAs of the species tested were probed using the D. D.Junebris — +? cardini group mauritiana sequences as a reference. In other words, if D. arawakana — a species contains some homologous sequences which quinaria group are homologous but diverged strongly from our refer- D. limbata — ence sequence, it will be difficult to detect them. That is Dorsilopha subgenus the reason why, complementing the classical analysis — — D. busckii +? by squash and Southern blots, some investigations by PCR amplification were performed using two sets of M & H Southern blot refers to the work of Maruyama & primers taken from regions suspected to evolve at a Hartl (1991a). slower rate than the other parts of the element. A blank means that the technique was not used. MARINER ELEMENTS IN THE DROSOPHILIDAE 383

Table 5 Distribution of the mariner element detected by three different techniques in the species of the Zaprionus genus and other related genera

Present study PCR M & H Squash blot Southern blot Species Southern blot (no. of bands) ITR INT

Zaprionus genus Zaprionus subgenus Z. indianus (Z.collarti) + + + 10—20 + (700bp) — Z. ornatus + + Z.spinipilus ++ 7-12 + + Z. vittiger ÷ + 15—20 + Z. (cf.) vittiger (Cape Town) + + Z. mascariensis - — 0 Z. sepsoldes — — 0 Z. tuberculatus + + + 2—7 + + Z. ghesquieri + + + 6—13 + + Z.inermis — — 0 + + Z. kolodkinae 36 Z.verruca ++ 2-3 +(l800bp) + Z. cercus 0 + + Anaprionus subgenus A. bogoriensis + + 5 A. lineosa 11 Chymomyza genus C. bicolor — — — Scaptodrosophila genus D. (cf) finitima — Scaptomyza genus Parascaptomyza subgenus S. pallida + +

M & H Southern blot refers to the work of Maruyama & Harth (199 la). A blank means that the technique was not used.

funebris obscura obscura ananassae quinaria robusta virilis

willistoni

saltans repleta

Fig. 4 Geographical distribution of the ananassae mariner-like elements based on the dis- melanogaster montium tribution of endemic species of the montium Drosophilidae family. zaprionus 384 F.BRUNETETAL.

present in the ancestor of the Drosophilidae family, Geographical distribution that it was lost in some lineages and was reacquired by Totry to understand the origin of the mariner element horizontal transmission. In this respect, analysing in the Drosophilidae family, its geographical distribu- mariner in other , Robertson (1993) showed the tion was analysed considering only endemic species. presence of different types of mariner in several This compilation, summarized in Fig. 4, shows that species suggesting the existence of several mariner sub- mariner is mainly present on the Asiatic and the families. Therefore, even if mariner were an ancient African continents. In other words, with the exception element, it could be reacquired several times from of species belonging to the obscura group, none of the several donors by horizontal transmission. Thus, we species endemic to the Palaearctic region and to the need more information, especially on sequence poly- American continent contains any mariner element morphism within and between more or less related hybridizing with the D. mauritiana probes. species.

Evolutionaryhypotheses Noteadded in proof Atleast two hypotheses may be proposed to interpret Thepresence of the mariner element in D. erecta the results. Firstly, the apparent random distribution (melanogaster subgroup) has been recently mentioned between species of this element and its restricted by A. R. Lohe, E. N. Moriyamo, D. A. Lidhoim and D. geographical distribution suggest the existence of hori- L. Hartl (manuscript submitted). The copies sequenced zontal transmission. Such a phenomenon has already are 97 per cent identical to those of the cat flea been proposed by Maruyama & Hartl (199 ib) to Ctenocephalides felis, and 50 per cent divergent from explain the high similarity observed between the the Mos-1 element of D. mauritiana. This result sequences of Zaprionus and some species of the strongly suggests the existence of horizontal transmis- melanogaster subgroup. However, to explain the sion. This could explain why these copies were not complete mariner distribution among the Drosophili- dae, it must be assumed that this phenomenon was detected with the mauritiana probes used in this work. relatively frequent. On the other hand, the geographical distribution restricted to the Asiatic and to the African Acknowledgements continents also suggests a repeated introduction of this element by horizontal transmission in species endemic Wethank the anonymous referees from their helpful comments. This work has benefitted from CNRS/NSF in these regions. The second hypothesis which can be proposed is (no. 693) and GREG (no. 48) grants. that the mariner element is an ancient element, as suggest by Kidwell (1993) and by Robertson (1993). In References this respect, assuming that a mariner element was present in the ancestor of the family Drosophilidae, the BRYAN,G. J., JACOBSON, J. W. AND HARTL, D. L. 1987. Heritable random distribution of this element among the species somatic excision of a Drosophila transposon. Science, of this family can be interpreted as the result of loss in 235, 1636—1638. some lineages. For instance, Kaplan et al. (1985) CAPY, P., ANXOLABEHERE, D. AND LANGIN, T. 1994. The strange showed that it is possible to lose a transposable phylogenies of transposable elements: are horizontal transfers the only explanation? Trends Genet., 10,7—12. element by genetic drift when the average number of DANIELS, 5. B., PETERSON, K. R., STRAUSBAUGH, L. D., KIDWELL, M. G. copies is relatively low. We also may consider that if, in AND CHOYNICK, A. 1990. Evidence for horizontal trans- a species, all the elements become inactive they will be mission of the P element between Drosophila species. easily lost by genetic drift. Genetics, 124, 339—355. Throckmorton (1975) and Wheeler (1981) GLOOR, G. AND ENGELS, w. 1991. Single- DNA preparations suggested that the origin of the Drosophilidae family for PCR. Drosph. Inf Serv., 17-18. was probably in south-east Asia. Therefore, the JACOBSON, J. W., MEDHORA, M. M. AND HARTL, D. L. 1986. Mole- hypothesis of an ancestral origin of the mariner cular structure of a somatically unstable element in Droso- element in this family is reinforced by its geographical phila. Proc. NatI. Acad. Sci. US.A., 83, 8684—8688. distribution. Indeed, it is quite possible that mariner KAPLAN, N., DARDEN T. AND LANGLEY, C. H. 1985. Evolution and extinction of transposable elements in Mendelian popula- was lost in several lineages during speciation, as stated tions. Genetics, 109,459—480. above, but also during the colonization of the new area. KIDWELL. M. G. 1993. Voyage of an ancient mariner. Nature, Thus, this could explain the absence of mariner in the 362, 202—202. Palaearctic region and on the American continent. LANGIN, T., CAPY, P. AND DABOUSSI, M. j.1994.The transposable These two hypotheses are not mutually exclusive element, Impala, a fungal member of the Tcl-mariner and it is quite possible that a mariner element was super family. Mo!. Gen. Genet. (in press). MARINER ELEMENTS IN THE DROSOPHILIDAE 385

LAWRENCE, J. G., OCHMAN, H. AND HARTL, D. L. 1992. The evolu- ROBERTSON, H. M. 1993. The mariner transposable element is tion of insertion sequences within enteric bacteria. widespread in insects. Nature, 362, 24 1—245. Genetics, 131, 9—20. SOUTHERN, E. M. 1975. Detection of specific sequences among LIDHOLM, D. A., GUDMUNDSSON, U. H. AND BOMAN, H, G. 1991. A DNA fragments separated by gel electrophoresis. .1. Mo!. highly repetitive mariner-like element in the genome of Biol., 98, 503—5 17. Hyalophora cecropia. J. Biol. Chem., 266, 11518—11521. TCHEN, P., ANXOLABEHRE, D., NOUAUD, D. AND PERIQUET, G. 1985. MARUYAMA, K. AND HARTL, D. L. 1991 a. Evolution of the trans- Hybridization on squashed flies: a method to detect genes posable element mariner in Drosophila species. Genetics, sequences in single Drosophila individuals. Analyt. 128, 319—329. Biochem., 150, 4 15—420. MARUYAMA, K. AND HARTL, D. L. 1991 b. Evidence for inter- THROCKMORTON, L.I-i. 1975. The phylogeny, ecology and specific transfer of the transposable element mariner geography of Drosophila. In: King, R. C. (ed.) Handbook between Drosophila and Zaprionus. J. Mo!. Evol., 33, of Genetics, vol. 3, pp.421—469. Plenum Press, New York. 514—524. WHEELER, M. R. 1981. The Drosophilidae: a taxonomic over- MIZROKHI, L. J. AND MAZO, A. M. 1990. Evidence for horizontal view. In: Ashburner, M., Carson H. L. and Thompson J. transmission of the mobile element jockey between distant N., Jr. The Genetics and Biology of Drosophila, vol. 3a, pp. Drosophila species. Proc. Nat!. Acad. Sci. U.S.A., 87, 1—97. Academic Press, New York. 92 16—9220.