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Evolution of the Transposable Element Mariner in Drosophila

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Evolution of the Transposable Element Mariner in Drosophila Copyright 8 1991 by the Genetics Society of America Evolution of the Transposable Elementmariner in Drosophila Species Kyoko Maruyama and Daniel L. Hart1 Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 631 10-1095 Manuscript received September 2 1, 1990 Accepted for publication February16, 199 1 ABSTRACT The distribution of the transposable elementmariner was examined in the genusDrosophila. Among the eight species comprisingthe melanogaster species subgroup,the element is present in D.mauritiana, D. simulans, D. sechellia, D.yakuba and D. teissieri, but it is absent in D. melanogaster, D. erecta and D. orena. Multiple copies ofmariner were sequenced from each species in whichthe element occurs.The inferred phylogenyof the elements andthe pattern of divergence were examined inorder to evaluate whether horizontal transfer among speciesor stochastic loss couldbetter account for the discontinuous distribution of the element amongthe species. The data suggest that the element was present in the ancestral species beforethe melanogaster subgroup diverged andwas lost in the lineage leading to D. melanogaster and the lineage leading to D. erecta and D. orena. This inference is consistent with the finding that mariner also occurs in members of several other species subgroups within the overall melanogaster species group, Within the melanogaster species subgroup, the average divergence of mariner copies between species was lower than the coding region of the alcohol dehydrogenase (Adh) gene. However, the divergence of mariner elements within species was as great as that observed for Adh. We conclude that the relative sequence homogeneityof mariner elements within species is more likely a result of rapid amplification of a few ancestral elements than of concerted evolution. The mariner element may also have had unequal mutation rates in different lineages. RANSPOSABLE elements comprise a class of ment in Drosophila. The P element appears to have T multigene families whose members are capable spread in Drosophila melanogaster only in the past few of moving from one chromosomallocation to another. decades, since it is prevalent in contemporary natural Although subject to extensive genetic and molecular populations but completely absent in old laboratory study,transposable elements are littleunderstood strains andin species closely related to D. melanogaster from the standpoint of evolutionary history. Trans- (KIDWELL1983). However, homologues of the P ele- posable elements can rapidly increase or decrease in ment are prevalent in more distantly related species copy numberwithout apparent phenotypic effects, comprising the willistoni and sultans species groups which distinguishes them from conventional single- (DANIELSet al. 1984; DANIELS and STRAUSBAUCH copy nuclear genes. A second distinction is that at 1986; LANSMANet al. 1987) [see ENGELS(1989) for least some transposable elements can undergo hori- review]. The discovery of a functional P element in zontal transfer between different species. For these D.willistoni that is virtually identical in nucleotide reasons and others, tranposable elements are subject sequence with the D. melanogaster element strongly to somewhat different evolutionary forces than con- argues that the elementwas transferred recently into ventional single-copy genes. the D. melanogaster genome from oneof these species Phylogenetic studies indicate that many transposa- (DANIELSet al. 1990). On the other hand,many trans- ble elements are distributed in discontinuous fashion posable elements reveal a more complex pattern in amongrelated taxa (DOWSETTand YOUNG 1982; their species distribution. For example, the transpos- MARTIN,WIERNASZ and SCHEDL1983; STACEYet al. ableelement designated I is also thought to have 1986). When a particular species lacks a transposable spread recently in populations ofD. melanogaster, sim- element that is found in closely related species, the ilar to thesituation with P. However, inactive elements finding is generally attributed to stochastic loss of the homologous to I are found in sibling species of D. element in the lineage of the particular species. Con- melanogaster, and it is not clear whether rapid spread versely, when a species contains a transposable ele- of the I element was initiated by interspecific transfer ment not foundin near relatives, the presence of the or whether some process allowed the activation of element is generally attributed to novel acquisition of previously inactive elements already in the genome theelement by interspecifictransfer from a more (BUCHETONet al. 1986) [see FINNEGAN(1989) for distantly related taxon. The occurrence of interspe- review]. cific transfer is illustrated by the P transposable ele- Inaddition to issues concerningthe distribution Genetics 128: 319-329 (June, 1991) 320 K. Maruyama and D. L. Hart1 and abundance of transposable elements, much re- A mains to be learned about forces governing the extent orena of nucleotidesequence variation between different crccrn copies of transposableelements within and among teissieri species. Although it has been suggested that dispersed, Y- moderately repetitive sequences mightundergo rapid concerted evolution as do tandemlyrepeated se- nulanogaster quences (ARNHEIM 1983),there is no strong evidence -sechellia for this view [see DOVER(1988) for review]. For the Simulnnr rDNA gene family in humans, it has been shown that -mnuriIia3u concerted evolution of rDNA sequences within the same chromosome is much more rapid than among B orena rDNA sequences in nonhomologouschromosomes erecta (SEPARACK,SLATKIN and ARNHEIM1988). In thecase of transposable elements, if sequences within a family teissieri are virtually identical, then this could result either - from concerted evolutionby specific genetic exchange melonogacrer mechanisms, such as gene conversion, or from recent amplification of a few ancestral copies of the element. -sechellia We report here a systematic study of the evolution Simulons of the transposable element mariner in the melano- -moluitiaM gaster species subgroup of Drosophila. The autono- FIGURE1.-Two alternative phylogenetic trees of the melano- mous mariner element is 1286 nucleotides in length, gaster species subgroup. Unequivocal relationships are indicated by thick lines and equivocal relationships by thin lines (redrawn from includes a single, long open reading frame encoding LACHAISEet al. 1988). a putative protein of 345 amino acids (presumed to be a transposase necessary for transposition), and has naturallyfound in D. melanogaster, D. erecta or D. terminal inverted repeats of 28 base pairs (JACOBSON, orena. MEDHORAand HARTL 1986). Eight species are as- Two hypotheses may be proposed to explain the signed to the melanogaster species subgroup, which discontinuous distribution of mariner in the melano- radiated in the Afro-tropical region. Two alternative gaster species subgroup. One model is that mariner trees have been proposed for the species phylogeny, was present in the common ancestor before the eight with three distinct species complexes recognized contemporary species divergedbut was lostin the within thesubgroup (Figure 1, modified from LA- lineages leading to D. orena, D. erecta and D. melano- gaster. If this model is correct, the gene phylogeny of CHAISE et al. 1988). Based on genetic distance data derived from allozymes and nucleotide sequences of mariner sequences among the species is expected to the Adh genes, the three complexes are thought to be congruent with the phylogeny of the species, and sequences homologous to mariner might be found in have split 6-15 million years ago (BODMERand ASH- other species related tothe melanogaster species BURNER 1984; LACHAISEet al. 1988). The species D. subgroup. The other model for the distribution of erecta and D. orena are restricted to a small part of mariner assumes that one or more recent horizontal Africa, whereas D. teissieri and D. yakuba are wide- transfers introduced the element into thefive species spread on the African mainland. These four species possessing it some time after the divergence of the are reproductively completely isolated from one an- subgroup began. Inthis case the phylogeny of mariner other, and they do not hybridize even in the labora- sequences would have no necessary correlation with tory. In the melanogaster species complex, D. sechellia the phylogeny of the species, andthe mariner se- and D. mauritiana are insular species (restricted to the quencesshould all be very similar to each other. Seychelles and Mauritius, respectively), while D. si- Although the models are not necessarily mutually mulans and D. melanogaster have spread worldwide. exclusive, the weight of the evidence may be deter- The three most closely related species are D. simulans, mined by comparing the phylogeny of mariner se- D. sechellia and D. mauritiana,and they produce fertile quences with the phylogeny of the species that contain female offspring when mated with each other (LA- them. These comparisons require knowledge of mar- CHAISE et al. 1988). Althoughthe mariner element was iner sequence variation, both within and between the first identified in D.mauritiana, homologous se- species in the subgroup. quences are also present in D. simulans, D. sechellia, We have carried out Southern blot hybridizations D. yakuba and D. teissieri. However, the species distri- on representative species of the major Drosophila spe- bution of mariner is discontinuous in that it is not cies groups in the
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