- Email: [email protected]
Horizontal transfer
Horizontal transfer Margaret G. Kidwell University of Arizona, Tucson, Arizona, USA Eukaryotic transposable elements provide some of the best documented examples of the occasional horizontal transfer of DNA sequences between both closely and distantly related species. Although the mechanisms involved in such a transfer remain a puzzle, new ideas are beginning to emerge. The rapidly expanding number of reports of transposable elements that may have been transferred horizontally raises questions both about whether these elements are more prone to this mode of transfer than non-mobile genes, and about the possible evolutionary significance if such a difference is real. Current Opinion in Genetics and Development 1992, 2:868-873
Introduction The vertical transmission of DNA or RNA sequences from parent to offspring provides the indisputable foundation for the genetic component of the evolution of life on earth. Nevertheless, it is now generally accepted that exceptions do occur in which sequences are transferred laterally, or horizontally, across taxonomic boundaries that at one time were considered by many to be inviolable. Hard proof for this mode of transfer in any particular instance is, however, often difficult to establish, and alternative hypotheses to explain incongruent observations can rarely be completely discounted. Several recent reviews of horizontal transfer [1-3] have tended to focus on the potential for gene transfer across large taxonomic distances by conjugative plasmids [4,5], with evidence accumulating for die mosaic structure of bacterial chromosomes [6,7], and an increasing understanding of the natural transfers that occur between Agrobacteria and plants [8]. I will, therefore, not attempt to cover these aspects here. Rather, I will focus on a spate of recent claims for possible horizontal transfer involving eukaryotic transposable genetic elements. I will then proceed to briefly discuss some general questions concerning the frequency, mechanisms, and significance of horizontal transfer, and the need for a logical, systematic approach to answer these questions.
Horizontal transfer among retroposons and retrotransposons Retroelements are DNA or RNA sequences that contain a gene encoding reverse transcriptase. They include both prokaryotic retrons and eukaryotic elements such as viruses, transposable elements, organelle introns and
plasmids. Retroposons and retrotransposons are transposable elements that, unlike retroviruses, generally do not construct virion particles, ~dthough some retrotransposons have been shown to form virus-like particles. The two types are distinguishable from one another in that retrotransposons have long terminal repeat (LTR) sequences, while retroposons lack these sequences. Previously, the alignment of protein sequences from a wide variety of eukaryotic retroelements [9,10] identified four branches of retroelements distinguishable by structural features, such as gene order, and the presence or absence of a spliced envelope protein. However, the data also indicated a number of unexpected events suggesting horizontal gene transfer. Recently tile evolutionaw relationships among the retroposons, and other retroelements have been investigated, on the basis of protein sequence alignment data [11o.] . Subsets of the retroposons apparently hm,e different assortments of retroviml-like genes. Consequently, phylogenies constructed from different individual genes are not always congruent with one another, suggesting xenologous recombination (the replacement of a resident gene by a homologous foreign gene) and/or independent gene assortment. Thus, there appears to have been occasional horizontal shuffling of gene sequence, and parts of gene sequences, among both closely and distantly related retroelements. A number of recent reports document tile widespread taxonomic distribution of two groups of retrotransposons, the T3,1-copia and Ty3-gl~osy groups. Genomic cop), number of these elements is often highly variable, but the frequency of active elements is low, particularly in plants [12o.,13]. The overall picture that is beginning to emerge from sequence comparisons is an interspersion of matching element and species phylogenies which is indicative of vertical transmission with evidence for sporadic putative horizontal transfer events,
Abbreviations Ac--Activator; LTR--Iong terminal repeat; MY--million years.
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Horizontal transfer Kidwell 869
often across wide phylogenetic distances. The similarity among retrotransposons isolated from species that have been separated for hundreds of millions of years is difficult to reconcile by any other mechanism, given the known high mutation rates of retroelements that use error-prone replication systems [9]. The T)*copia group of retrotransposons provides some of the best documented evidence for horizontal transfer of retrotransposons across kingdom boundaries. Earlier it was demonstrated [14] that the retrotransposons Ta 8-10 of Arabidopsis thaliana are more similar in sequence to the Drosophila melanogaster elements copia and 1731 than they are to other elements in the A. thaliana genome. Flavell el aL [15o.,16 ,,] have now shown that, along with the extreme heterogeneity of Tyl-copia elements in flowering plants and other invertebrate eukaryotes, there are many ex,'maples in which the degree of divergence between element sequences bears little relation to the phylogenetic distances between the host species. The presence of a retrotransposon, Tchl, in a vertebrate species, the herring (Clttpea harengus), has also been demonstrated [17"] and provides further evidence suggestive of horizontal transfer. A number of additional instances of a similar discordance between retrotransposon phylogenies mad those of their hosts is provided by the Ty3-gO~0s3~group. For exanaple, on the basis of phylogenetic reconstruction, the plant elements IFG7 ( from Pinus radiata) and dell (from Lilium henryi) appear to be more closely related to the Ty3 element of yeast, and to several insect elements, than they are to other plant elements [10]. The analysis of g)ps3p elements within species of the Drosophila t,irilis group [18] suggested that divergence of amino-acid sequences was of the same order of magnitude as that between nonmobile genes in these species (20--40%). In this case, the argument for horizontal transfer, based on an expected faster divergence rate in active retrotransposons than in non-mobile genes, is not as strong as in the previous examples.
Multiple transposable-element invasions in Drosophila
,
Recent reports provide additional support for the earlier proposal [19] that active transposable elements have invaded the cosmopolitan species D. melanogaster during the past half century. There is now good evidence for the recent invasion of this species by the hobo element, in addition to that by P and active I elements. In contrast to P and hobo elements, which have short inverted terminal repeats, the I element is a retroelement with a structure similar to that of mammalian LINES (long interspersed elements). Although, as described below, a good case can be made for the introduction of P and hobo into D. melanogasterby horizontal transfer, it is not clear whether horizontal transfer, introgressive hybridization or other mechanisms were responsible for the reintroduction of active/elements into D. melanogaster [20"].
The most compelling case for the occurrence of horizontal transfer in any eukaryotic system is provided by the P element [21,]. In addition to evidence for the recent introduction and spread of P elements in 19. melanogaster and the patchy distribution of P elements in the genus Drosophila, the dramatic incongruity of the near-identity of/). melanogasterand D. wilistoni P-element sequences with the greater than 50 million years (MY) divergence time of their host species [22] is virtually impossible to explain by a w other mechanism. New data from D. b(7"asciata [23"] and Scaptomyza [24"] give further weight to tile validity of this hypothesis. Also, the detection of P-homologous sequences in the blow fly [25] opens up a much broader phylogenetic range for the direction of future studies. In the case of the hobo element, evidence for recent invasion of D. melanogaster comes from the distribution patterns of active and inactive elements [26,27]. New data on hobo DNA sequences from the sibling species D. melanogaster, Drosophila simulans and Drosophila maur#iana reveal an extremely low level of sequence divergence that is consistent with recent horizontal transfer into, or anaong, these species [28..]. In a similar way, but from a phylogenetically much broader perspective, it has been detem~ined that the transposase sequences of hobo from D. melanogaste,, Activator (Ac) from maize, and Tam3 from Antim'hinum majus show a considerably greater sequence similarity than expected from the long period of time since the divergence of the lineages that gave rise to their host species [29,30"]. However, in a stud), of maize and pearl millet sequences [31"], the rate of divergence of Aolike elements was similar to that of the non-mobile gene Adhl, suggesting that these elements shared a common ancestor prior to the plant-animal split, rather than a recent acquisition of Ac by pearl millet from maize. The mariner element is broadly distributed in the melanogaster species group of Drosophila, but outside the Drosophilids a high degree of sequence similarity is found only in the genus Zaprionus. Although the distribution of mariner within species of the melanogaster group of Drosophila may be better explained by vertical than horizontal transfer [32o], when sequences from Zaprionus tuberculatus are included, incongruities between mariner and Adh (which encodes alcohol dehydrogenase) phylogenies strongly suggest horizontal transfer [33"]. The finding of mariner-like sequences in the moth, Hyalophora cecropia, with an overall 48% sequence similarity to the mariner element of D. mauritiana [34] suggests the possibility of horizontal transfer between even more distantly related species. The elements Tcl and Tbl from Caenorbabditis ele~ gans and Caenorhabditis briggsae have sequence similarity with the HB1 element of 19. melanogaster and the Ubu element of the Hawaiian Drosophila species D. heteroneura. The result of comparisons of element sequences from this family have been interpreted in terms of strictly vertical transfer [35,36]. However, it is not clear that appropriate comparisons with the phylogenies of other genes have always been made. Study of the distribution of sequences homologous to six el-
870 Genomesand evolution ements from C. elegans [37"] have indicated different patterns of distribution. Some of these differences are readily explained by vertical transmission, while others suggest that horizontal transmission might have occurred. The recent report of a Tcl-like sequence in catfish [38] extends the scope of future phylogenetic studies of this class of element.
Do transposable elements transfer horizontally more frequently than non-mobile genes? The recent flurry of reports suggesting horizontal transfer of transposable elements appears to be in contrast to the seeming rarity of similar reports for non-transposing sequences. This raises the question of whether these elements transfer laterally more frequently than do 'non-mobile' genes, or whether unequal sanlpling, or some other explanation might explain the discrepancT. The specific adaptations of transposable elements for movement within and between genomes would seem to give them an important edge with respect to horizontal transfer. The flood of new DNA sequence data that is emerging should provide estinaates of the relative frequencies of horizontal transfer for different types of sequences as based on adequate sanaples.
Mechanisms for horizontal transfer Until recently the paucity of plausible mechanisnas for the mediation of horizontal transfer, particularly in complex eukaryotes, has often been a major obstacle to considering such a possibility. Based on prokaryotic models, the potential for horizontal transfer by means of plasmidmediated conjugation, even between different kingdonas, has recently been widely discussed [1,2,4,5]. In addition, based on evidence for the mosaic structure of chromosomes, transfomaation appears to be a common mode of transfer between bacterial lineages [6], although phagemediated transduction, or plasmid-mediated conjugation, are more likely mechanisms in bacterial species that do not possess natural competence for transformation [39[. However, our understanding of the mechanisms involved in mediating horizontal transfer in eukaryotic genomes is currently extremely limited. Certain characteristics of viruses appear to make them suitable to act as shuttles for horizontal transfer by the passive transduction of host genes in a viral capsid [40] and there have been a number of earlier reports of transposable elements being carried by viruses [41,42]. However, host specificity of viruses may be an important obstacle for mediating transfers across wide taxonomic distances and, to date, there appears to be no hard evidence for their ability to perform this role in eukaryotic systems. Interest in larger and more complex parasitic vectors as possible agents for horizontal transfer has recently
been sparked by the demonstration that a semi-parasitic mite, Proctolaelaps regalis, can carry P.element DNA sequences after feeding on Drosophila that contain P elements [43"]. Furthermore, the feeding behavior and geographical range of this parasite are consistent with the possibility that it may have acted as a vector for the purported interspecific horizontal transfer of P sequences between D. willistoni and D. melanogaster [21",22].
The evolutionary role of horizontal transfer While it appears that the general evolutionary significance of transposable elements [44] will co,ltinue to be body debated, emerging information about tile horizontal transfer of these sequences m w provide new insights into this question. For exan~ple, the ability of an element to transpose, stably h~tegrate, and replicate in a new host species could provide an important longterm evok~tionary advantage to transposable secluences whose evolutionary history may include the eventual loss of transpositional ability and final extinction [45"]. Horizontal transfer offers such sequences the promise of immort~dity, which may be particularly impommt for the long-tem~ survival of parasitic sequences that cannot expect to survive over long periods of evolutionary time by virtue of any selective advantage that they might confer on their hosts. Incidentally, in prokaryotes, plasmidmediated horizontal transmission probably imposes a selection against non-autonomous elements, as this type of element is incapable of mobilizing itself [45"]. Previously, a number of mechanisms have been suggested by which dispersed repeated elements might interact with their hosts in, at least, a transitory symbiotic relationship [44]. For example, it has been argued [46"] that repeated sequences might provide the 'bricks and mortar' for the observed high variability in genome size in many plants. Although the significance of such variability is not presently understood, the idea that it could be subject to selective forces because of the correlation between genome size, ceil size and various asl)ects of plant life form, such as growth rate and developmental time [47], deserves serious consideration. Ho,izontal transfer of sequences could thus play an important role in adaptive evolution, if transfer occurs :it sutt~ciently high frequencies. The possibility of a significantly higher frequencT of horizontal transfer of eukaryotic mobile elements, relative to that of their hosts' genes, is reminiscent of the mosaic structure of bacterial genomes in which clonal frames, that have been vertically inherited, are interspersed with recombinant sequences brought into the chromosome by horizontal transfer [7]. If non-mobile eukaryotic genes are transmitted vertically, with very few exceptions, this would lead to congruent phylogenies among the vast majori W of genes in the same lineage. This might be in contrast to the occasional horizontal transfer of repetitive DNA, including transposable elements, that would constitute a portion of genomes that is fluid, both with respect to movement and recombination of these se-
Horizontal transfer Kidwell 871 quences within genomes and species, but also among reproductively isolated taxa. The evolutionary implications of relatively frequent horizontal transfer of repetitive sequences, embedded in a stable matrix of conventional genes, would perhaps be limited in comparison with a scenario in which all genes might occasionally be subjected to such transfer. However, a mosaic-like structure could provide occasional benefits of 'interkingdom sex' within an overall stable genomic framework.
New methodologies for the study of horizontal transfer Better methods, both experimental and statistical, for stud}4ng horizontal transfer need developing, to replace the somewhat haphazard, and often serendipitous, way daat these events previously canae to the attention of researchers. A better understanding of horizontal transfer should be facilitated by well planned, detailed molecular .systematic studies such as those described for plants [48.] and enteric bacteria [49"]. Implicit in this approach is the construction and comparison of gene and species phylogenetic trees based on different genes from the same species. In addition, the theoretical exploration and development of statistical methods to detect patterns of incongruiW between gene and species trees are needed. These should separate the incongruities resulting from horizontal transfer events from those that result from other causes, such as Iwbridization or unequal rates of evolution. A start has been made in the development of statistic,-d approaches to these questions. For example, use of the 'C' statistics program led to the obseta,ation of discrepancies in codon usages between a nun> ber of Dro ophila transposable elements and their host genomes [50]. Mso, a class of genes that were identified on the basis of differential codon usage, may have been acquired by horizontal transfer and rnay be involved in bacterial speciation [51]. In addition, a potentially useful non-parametric statistical method, based on nucleotide comparisons, has recently been developed for determining the statistical significance of suspected inconsistencies in taxonomic relationships [52"].
understand the mechanisms, frequency and broad evolutionary significance of these phenomena.
Acknowledgements I thank David Finnegan, Jon Clark, Michael Donoghue and Martin Woiciechowski for discussions and for critical reading of this manuscript. This work was supported by grant DEB-9119349 from the National Science Foundation.
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MG Kidwell, Department of Ecology and Evolutionary Biology, Universit), of Arizona, Tucson, Arizona 85721, USA.
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Introduction The vertical transmission of DNA or RNA sequences from parent to offspring provides the indisputable foundation for the genetic component of the evolution of life on earth. Nevertheless, it is now generally accepted that exceptions do occur in which sequences are transferred laterally, or horizontally, across taxonomic boundaries that at one time were considered by many to be inviolable. Hard proof for this mode of transfer in any particular instance is, however, often difficult to establish, and alternative hypotheses to explain incongruent observations can rarely be completely discounted. Several recent reviews of horizontal transfer [1-3] have tended to focus on the potential for gene transfer across large taxonomic distances by conjugative plasmids [4,5], with evidence accumulating for die mosaic structure of bacterial chromosomes [6,7], and an increasing understanding of the natural transfers that occur between Agrobacteria and plants [8]. I will, therefore, not attempt to cover these aspects here. Rather, I will focus on a spate of recent claims for possible horizontal transfer involving eukaryotic transposable genetic elements. I will then proceed to briefly discuss some general questions concerning the frequency, mechanisms, and significance of horizontal transfer, and the need for a logical, systematic approach to answer these questions.
Horizontal transfer among retroposons and retrotransposons Retroelements are DNA or RNA sequences that contain a gene encoding reverse transcriptase. They include both prokaryotic retrons and eukaryotic elements such as viruses, transposable elements, organelle introns and
plasmids. Retroposons and retrotransposons are transposable elements that, unlike retroviruses, generally do not construct virion particles, ~dthough some retrotransposons have been shown to form virus-like particles. The two types are distinguishable from one another in that retrotransposons have long terminal repeat (LTR) sequences, while retroposons lack these sequences. Previously, the alignment of protein sequences from a wide variety of eukaryotic retroelements [9,10] identified four branches of retroelements distinguishable by structural features, such as gene order, and the presence or absence of a spliced envelope protein. However, the data also indicated a number of unexpected events suggesting horizontal gene transfer. Recently tile evolutionaw relationships among the retroposons, and other retroelements have been investigated, on the basis of protein sequence alignment data [11o.] . Subsets of the retroposons apparently hm,e different assortments of retroviml-like genes. Consequently, phylogenies constructed from different individual genes are not always congruent with one another, suggesting xenologous recombination (the replacement of a resident gene by a homologous foreign gene) and/or independent gene assortment. Thus, there appears to have been occasional horizontal shuffling of gene sequence, and parts of gene sequences, among both closely and distantly related retroelements. A number of recent reports document tile widespread taxonomic distribution of two groups of retrotransposons, the T3,1-copia and Ty3-gl~osy groups. Genomic cop), number of these elements is often highly variable, but the frequency of active elements is low, particularly in plants [12o.,13]. The overall picture that is beginning to emerge from sequence comparisons is an interspersion of matching element and species phylogenies which is indicative of vertical transmission with evidence for sporadic putative horizontal transfer events,
Abbreviations Ac--Activator; LTR--Iong terminal repeat; MY--million years.
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Horizontal transfer Kidwell 869
often across wide phylogenetic distances. The similarity among retrotransposons isolated from species that have been separated for hundreds of millions of years is difficult to reconcile by any other mechanism, given the known high mutation rates of retroelements that use error-prone replication systems [9]. The T)*copia group of retrotransposons provides some of the best documented evidence for horizontal transfer of retrotransposons across kingdom boundaries. Earlier it was demonstrated [14] that the retrotransposons Ta 8-10 of Arabidopsis thaliana are more similar in sequence to the Drosophila melanogaster elements copia and 1731 than they are to other elements in the A. thaliana genome. Flavell el aL [15o.,16 ,,] have now shown that, along with the extreme heterogeneity of Tyl-copia elements in flowering plants and other invertebrate eukaryotes, there are many ex,'maples in which the degree of divergence between element sequences bears little relation to the phylogenetic distances between the host species. The presence of a retrotransposon, Tchl, in a vertebrate species, the herring (Clttpea harengus), has also been demonstrated [17"] and provides further evidence suggestive of horizontal transfer. A number of additional instances of a similar discordance between retrotransposon phylogenies mad those of their hosts is provided by the Ty3-gO~0s3~group. For exanaple, on the basis of phylogenetic reconstruction, the plant elements IFG7 ( from Pinus radiata) and dell (from Lilium henryi) appear to be more closely related to the Ty3 element of yeast, and to several insect elements, than they are to other plant elements [10]. The analysis of g)ps3p elements within species of the Drosophila t,irilis group [18] suggested that divergence of amino-acid sequences was of the same order of magnitude as that between nonmobile genes in these species (20--40%). In this case, the argument for horizontal transfer, based on an expected faster divergence rate in active retrotransposons than in non-mobile genes, is not as strong as in the previous examples.
Multiple transposable-element invasions in Drosophila
,
Recent reports provide additional support for the earlier proposal [19] that active transposable elements have invaded the cosmopolitan species D. melanogaster during the past half century. There is now good evidence for the recent invasion of this species by the hobo element, in addition to that by P and active I elements. In contrast to P and hobo elements, which have short inverted terminal repeats, the I element is a retroelement with a structure similar to that of mammalian LINES (long interspersed elements). Although, as described below, a good case can be made for the introduction of P and hobo into D. melanogasterby horizontal transfer, it is not clear whether horizontal transfer, introgressive hybridization or other mechanisms were responsible for the reintroduction of active/elements into D. melanogaster [20"].
The most compelling case for the occurrence of horizontal transfer in any eukaryotic system is provided by the P element [21,]. In addition to evidence for the recent introduction and spread of P elements in 19. melanogaster and the patchy distribution of P elements in the genus Drosophila, the dramatic incongruity of the near-identity of/). melanogasterand D. wilistoni P-element sequences with the greater than 50 million years (MY) divergence time of their host species [22] is virtually impossible to explain by a w other mechanism. New data from D. b(7"asciata [23"] and Scaptomyza [24"] give further weight to tile validity of this hypothesis. Also, the detection of P-homologous sequences in the blow fly [25] opens up a much broader phylogenetic range for the direction of future studies. In the case of the hobo element, evidence for recent invasion of D. melanogaster comes from the distribution patterns of active and inactive elements [26,27]. New data on hobo DNA sequences from the sibling species D. melanogaster, Drosophila simulans and Drosophila maur#iana reveal an extremely low level of sequence divergence that is consistent with recent horizontal transfer into, or anaong, these species [28..]. In a similar way, but from a phylogenetically much broader perspective, it has been detem~ined that the transposase sequences of hobo from D. melanogaste,, Activator (Ac) from maize, and Tam3 from Antim'hinum majus show a considerably greater sequence similarity than expected from the long period of time since the divergence of the lineages that gave rise to their host species [29,30"]. However, in a stud), of maize and pearl millet sequences [31"], the rate of divergence of Aolike elements was similar to that of the non-mobile gene Adhl, suggesting that these elements shared a common ancestor prior to the plant-animal split, rather than a recent acquisition of Ac by pearl millet from maize. The mariner element is broadly distributed in the melanogaster species group of Drosophila, but outside the Drosophilids a high degree of sequence similarity is found only in the genus Zaprionus. Although the distribution of mariner within species of the melanogaster group of Drosophila may be better explained by vertical than horizontal transfer [32o], when sequences from Zaprionus tuberculatus are included, incongruities between mariner and Adh (which encodes alcohol dehydrogenase) phylogenies strongly suggest horizontal transfer [33"]. The finding of mariner-like sequences in the moth, Hyalophora cecropia, with an overall 48% sequence similarity to the mariner element of D. mauritiana [34] suggests the possibility of horizontal transfer between even more distantly related species. The elements Tcl and Tbl from Caenorbabditis ele~ gans and Caenorhabditis briggsae have sequence similarity with the HB1 element of 19. melanogaster and the Ubu element of the Hawaiian Drosophila species D. heteroneura. The result of comparisons of element sequences from this family have been interpreted in terms of strictly vertical transfer [35,36]. However, it is not clear that appropriate comparisons with the phylogenies of other genes have always been made. Study of the distribution of sequences homologous to six el-
870 Genomesand evolution ements from C. elegans [37"] have indicated different patterns of distribution. Some of these differences are readily explained by vertical transmission, while others suggest that horizontal transmission might have occurred. The recent report of a Tcl-like sequence in catfish [38] extends the scope of future phylogenetic studies of this class of element.
Do transposable elements transfer horizontally more frequently than non-mobile genes? The recent flurry of reports suggesting horizontal transfer of transposable elements appears to be in contrast to the seeming rarity of similar reports for non-transposing sequences. This raises the question of whether these elements transfer laterally more frequently than do 'non-mobile' genes, or whether unequal sanlpling, or some other explanation might explain the discrepancT. The specific adaptations of transposable elements for movement within and between genomes would seem to give them an important edge with respect to horizontal transfer. The flood of new DNA sequence data that is emerging should provide estinaates of the relative frequencies of horizontal transfer for different types of sequences as based on adequate sanaples.
Mechanisms for horizontal transfer Until recently the paucity of plausible mechanisnas for the mediation of horizontal transfer, particularly in complex eukaryotes, has often been a major obstacle to considering such a possibility. Based on prokaryotic models, the potential for horizontal transfer by means of plasmidmediated conjugation, even between different kingdonas, has recently been widely discussed [1,2,4,5]. In addition, based on evidence for the mosaic structure of chromosomes, transfomaation appears to be a common mode of transfer between bacterial lineages [6], although phagemediated transduction, or plasmid-mediated conjugation, are more likely mechanisms in bacterial species that do not possess natural competence for transformation [39[. However, our understanding of the mechanisms involved in mediating horizontal transfer in eukaryotic genomes is currently extremely limited. Certain characteristics of viruses appear to make them suitable to act as shuttles for horizontal transfer by the passive transduction of host genes in a viral capsid [40] and there have been a number of earlier reports of transposable elements being carried by viruses [41,42]. However, host specificity of viruses may be an important obstacle for mediating transfers across wide taxonomic distances and, to date, there appears to be no hard evidence for their ability to perform this role in eukaryotic systems. Interest in larger and more complex parasitic vectors as possible agents for horizontal transfer has recently
been sparked by the demonstration that a semi-parasitic mite, Proctolaelaps regalis, can carry P.element DNA sequences after feeding on Drosophila that contain P elements [43"]. Furthermore, the feeding behavior and geographical range of this parasite are consistent with the possibility that it may have acted as a vector for the purported interspecific horizontal transfer of P sequences between D. willistoni and D. melanogaster [21",22].
The evolutionary role of horizontal transfer While it appears that the general evolutionary significance of transposable elements [44] will co,ltinue to be body debated, emerging information about tile horizontal transfer of these sequences m w provide new insights into this question. For exan~ple, the ability of an element to transpose, stably h~tegrate, and replicate in a new host species could provide an important longterm evok~tionary advantage to transposable secluences whose evolutionary history may include the eventual loss of transpositional ability and final extinction [45"]. Horizontal transfer offers such sequences the promise of immort~dity, which may be particularly impommt for the long-tem~ survival of parasitic sequences that cannot expect to survive over long periods of evolutionary time by virtue of any selective advantage that they might confer on their hosts. Incidentally, in prokaryotes, plasmidmediated horizontal transmission probably imposes a selection against non-autonomous elements, as this type of element is incapable of mobilizing itself [45"]. Previously, a number of mechanisms have been suggested by which dispersed repeated elements might interact with their hosts in, at least, a transitory symbiotic relationship [44]. For example, it has been argued [46"] that repeated sequences might provide the 'bricks and mortar' for the observed high variability in genome size in many plants. Although the significance of such variability is not presently understood, the idea that it could be subject to selective forces because of the correlation between genome size, ceil size and various asl)ects of plant life form, such as growth rate and developmental time [47], deserves serious consideration. Ho,izontal transfer of sequences could thus play an important role in adaptive evolution, if transfer occurs :it sutt~ciently high frequencies. The possibility of a significantly higher frequencT of horizontal transfer of eukaryotic mobile elements, relative to that of their hosts' genes, is reminiscent of the mosaic structure of bacterial genomes in which clonal frames, that have been vertically inherited, are interspersed with recombinant sequences brought into the chromosome by horizontal transfer [7]. If non-mobile eukaryotic genes are transmitted vertically, with very few exceptions, this would lead to congruent phylogenies among the vast majori W of genes in the same lineage. This might be in contrast to the occasional horizontal transfer of repetitive DNA, including transposable elements, that would constitute a portion of genomes that is fluid, both with respect to movement and recombination of these se-
Horizontal transfer Kidwell 871 quences within genomes and species, but also among reproductively isolated taxa. The evolutionary implications of relatively frequent horizontal transfer of repetitive sequences, embedded in a stable matrix of conventional genes, would perhaps be limited in comparison with a scenario in which all genes might occasionally be subjected to such transfer. However, a mosaic-like structure could provide occasional benefits of 'interkingdom sex' within an overall stable genomic framework.
New methodologies for the study of horizontal transfer Better methods, both experimental and statistical, for stud}4ng horizontal transfer need developing, to replace the somewhat haphazard, and often serendipitous, way daat these events previously canae to the attention of researchers. A better understanding of horizontal transfer should be facilitated by well planned, detailed molecular .systematic studies such as those described for plants [48.] and enteric bacteria [49"]. Implicit in this approach is the construction and comparison of gene and species phylogenetic trees based on different genes from the same species. In addition, the theoretical exploration and development of statistical methods to detect patterns of incongruiW between gene and species trees are needed. These should separate the incongruities resulting from horizontal transfer events from those that result from other causes, such as Iwbridization or unequal rates of evolution. A start has been made in the development of statistic,-d approaches to these questions. For example, use of the 'C' statistics program led to the obseta,ation of discrepancies in codon usages between a nun> ber of Dro ophila transposable elements and their host genomes [50]. Mso, a class of genes that were identified on the basis of differential codon usage, may have been acquired by horizontal transfer and rnay be involved in bacterial speciation [51]. In addition, a potentially useful non-parametric statistical method, based on nucleotide comparisons, has recently been developed for determining the statistical significance of suspected inconsistencies in taxonomic relationships [52"].
understand the mechanisms, frequency and broad evolutionary significance of these phenomena.
Acknowledgements I thank David Finnegan, Jon Clark, Michael Donoghue and Martin Woiciechowski for discussions and for critical reading of this manuscript. This work was supported by grant DEB-9119349 from the National Science Foundation.
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MG Kidwell, Department of Ecology and Evolutionary Biology, Universit), of Arizona, Tucson, Arizona 85721, USA.
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