Ancestral polymorphism and recent invasion of transposable elements in Drosophila species

BMC Evolutionary Biology

Claudia Marcia Aparecida Carareto¹  Elaine Silva Dias¹ 

[1] Department of Biology, São José do Rio Preto, UNESP - São Paulo State University, São Paulo, Brazil

关键词: Drosophila melanogaster group;    Recent invasion;    Introgressive hybridization;    Horizontal transfer;    Ancestral polymorphism;    Transposable elements;   

Others  :  1140779
DOI  :  10.1186/1471-2148-12-119

 received in 2011-12-09, accepted in 2012-07-10,  发布年份 2012

【 摘 要 】

Background

During the evolution of transposable elements, some processes, such as ancestral polymorphisms and horizontal transfer of sequences between species, can produce incongruences in phylogenies. We investigated the evolutionary history of the transposable elements Bari and 412 in the sequenced genomes of the Drosophila melanogaster group and in the sibling species D. melanogaster and D. simulans using traditional phylogenetic and network approaches.

Results

Maximum likelihood (ML) phylogenetic analyses revealed incongruences and unresolved relationships for both the Bari and 412 elements. The DNA transposon Bari within the D. ananassae genome is more closely related to the element of the melanogaster complex than to the sequence in D. erecta, which is inconsistent with the species phylogeny. Divergence analysis and the comparison of the rate of synonymous substitutions per synonymous site of the Bari and host gene sequences explain the incongruence as an ancestral polymorphism that was inherited stochastically by the derived species. Unresolved relationships were observed in the ML phylogeny of both elements involving D. melanogaster, D. simulans and D. sechellia. A network approach was used to attempt to resolve these relationships. The resulting tree suggests recent transfers of both elements between D. melanogaster and D. simulans. The divergence values of the elements between these species support this conclusion.

Conclusions

We showed that ancestral polymorphism and recent invasion of genomes due to introgression or horizontal transfer between species occurred during the evolutionary history of the Bari and 412 elements in the melanogaster group. These invasions likely occurred in Africa during the Pleistocene, before the worldwide expansion of D. melanogaster and D. simulans.

【 授权许可】

   
2012 Dias and Carareto; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Lerman D, Michalak P, Helin A, Bettencourt B, Feder M: Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol Biol Evol 2003, 20:135-144.
• [2]Bejerano G, Lowe C, Ahituv N, King B, Siepel A, Salama S, Rubin E, Kent W, Haussler D: A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 2006, 441:87-90.
• [3]Feschotte C: Opinion - Transposable elements and the evolution of regulatory networks. Nat Rev Genet 2008, 9:397-405.
• [4]Nakayashiki H: The Trickster in the genome: contribution and control of transposable elements. Genes Cells 2011, 16:827-841.
• [5]Almeida LM, Carareto CMA: Origem, Proliferação e Extinção de Elementos de Transponíveis: Qual Seria a Importância da Transferência Horizontal na Manutenção desse Ciclo? Série Monografias, SBG, Ribeirão Preto 2005, 1:1-40.
• [6]Capy P, Langin T, Anxolabehere D, Bazin C: Dynamics and Evolution of Transposable Elements. 1st edition. Austin: Landes Bioscience; 1998.
• [7]Schaack S, Gilbert C, Feschotte C: Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. Trends Ecol Evol 2010, 25:537-546.
• [8]Loreto ELS, Carareto CMA, Capy P: Revisiting horizontal transfer of transposable elements in Drosophila. Heredity 2008, 100:545-554.
• [9]Carareto C: Tropical Africa as a cradle for horizontal transfers of transposable elements between species of the genus Drosophila and Zaprionus. Mobile Genetics Elements 2011, 2:179-186.
• [10]Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, Ashburner M: Historical biogeography of the Drosophila melanogaster species subgroup. Evolutionary Biology 1988, 22:159-225.
• [11]Hey J, Kliman RM: Population Genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol 1993, 10:804-822.
• [12]Lachaise D, Silvain J: How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 2004, 120:17-39.
• [13]van der Linde K, Houle D: A supertree analysis and literature review of the genus Drosophila and closely related genera (Diptera, Drosophilidae). Insect Systematics & Evolution 2008, 39:241-267.
• [14]Yang Y, Hou Z-C, Qian Y-H, Kang H, Zeng Q-T: Increasing the data size to accurately reconstruct the phylogenetic relationships between nine subgroups of the Drosophila melanogaster species group (Drosophilidae, Diptera). Mol Phylogenet Evol 2012, 62:214-223.
• [15]Dobzhansky T, Dreyfus A: Chromosomal aberrations in Brazilian Drosophila ananassae. Proc Natl Acad Sci 1943, 29:301-305.
• [16]Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, et al.: Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450:203-218.
• [17]Das A: Population genomic and bioinformatic studies reveal evolutionary history of Drosophila ananassae. Curr Sci 2005, 89:1316-1321.
• [18]Sanchez-Gracia A, Maside X, Charlesworth B: High rate of horizontal transfer of transposable elements in Drosophila. Trends Genet 2005, 24:200-203.
• [19]Bartolome C, Bello X, Maside X: Widespread evidence for horizontal transfer of transposable elements across Drosophila genomes. Genome Biol 2009, 10:R22. BioMed Central Full Text
• [20]Lerat E, Burlet N, Biémont C, Vieira C: Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 2010, 473:100-109.
• [21]Caizzi R, Caggese C, Pimpinelli S: Bari-1, a new transposon-like family in Drosophila melanogaster with a unique heterochromatic organization. Genetics 1993, 133:335-345.
• [22]Moschetti R, Caggese C, Barsanti P, Caizzi R: Intra- and interspecies variation among Bari-1 elements of the melanogaster species group. Genetics 1998, 150:239-250.
• [23]Moschetti R, Chlamydas S, Marsano R, Caizzi R: Conserved motifs and dynamic aspects of the terminal inverted repeat organization within Bari-like transposons. Mol Genet Genomics 2008, 279:451-461.
• [24]Mugnier N, Biemont C, Vieira C: New regulatory regions of Drosophila 412 retrotransposable element generated by recombination. Mol Biol Evol 2005, 22:747-757.
• [25]Tamura K, Subramanian S, Kumar S: Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks. Mol Biol Evol 2004, 21:36-44.
• [26]Posada D, Crandall K: Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 2001, 16:37-45.
• [27]Cordaux R, Hedges DJ, Batzer MA: Retrotransposition of Alu elements: how many sources? Trends Genet 2004, 20:464-467.
• [28]Da Lage J, Kergoat G, Maczkowiak F, Silvain J, Cariou M, Lachaise D: A phylogeny of Drosophilidae using the Amyrel gene: questioning the Drosophila melanogaster species group boundaries. Journal of Zoological Systematics and Evolutionary Research 2007, 45:47-63.
• [29]Bowen N, McDonald J: Drosophila Euchromatic LTR Retrotransposons are Much Younger Than the Host Species in Which They Reside. Genome Res 2001, 11:1527-1540.
• [30]Mugnier N, Gueguen L, Vieira C, Biemont C: The heterochromatic copies of the LTR retrotransposons as a record of the genomic events that have shaped the Drosophila melanogaster genome. Gene 2008, 411:87-93.
• [31]Cizeron G, Lemeunier F, Loevenbruck C, Brehm A, Biemont C: Distribution of the retrotransposable element 412 in Drosophila species. Mol Biol Evol 1998, 15:1589-1599.
• [32]Caggese C, Pimpinelli S, Barsanti P, Caizzi R: The distribution of the transposable element Bari-1 in the Drosophila melanogaster and Drosophila simulans genomes. Genetica 1995, 96:269-283.
• [33]Russo C, Takezaki N, Nei M: Molecular phylogeny and divergence times of Drosophilid species. Mol Biol Evol 1995, 12:391-404.
• [34]Maruyama K, Hartl DL: Evidence for interspecific transfer of the transposable element mariner between Drosophila and Zaprionus. J Mol Evol 1991, 33:514-524.
• [35]Bregliano JC, Kidwell MG (Eds): Hybrid dysgenesis determinants. New York: Academic Pres; 1983.
• [36]Jordan IK, Matyunina LV, McDonald JF: Evidence for the recent horizontal transfer of long terminal repeat retrotransposon. Proc Natl Acad Sci USA 1999, 96:12621-12625.
• [37]Sanchez-Gracia A, Maside X, Charlesworth B: High rate of horizontal transfer of transposable elements in Drosophila. Trends Genet 2005, 21:200-203.
• [38]Ludwig A, Valente V, Loreto ELS: Multiple invasions of Errantivirus in the genus Drosophila. Insect Mol Biol 2008, 17:113-124.
• [39]Vidal NM, Ludwig A, Loreto ELS: Evolution of Tom, 297, 17.6 and rover retrotransposons in Drosophilidae species. Mol Genet Genomics 2009, 282:351-362.
• [40]Depra M, Valente VLD, Margis R, Loreto ELS: The hobo transposon and hobo-related elements are expressed as developmental genes in Drosophila. Gene 2009, 448:57-63.
• [41]de Setta N, Van Sluys MA, Capy P, Carareto CMA: Multiple invasions of Gypsy and Micropia retroelements in genus Zaprionus and melanogaster subgroup of the genus Drosophila. BMC Evol Biol 2009, 9:279. BioMed Central Full Text
• [42]Lerat E, Burlet N, Biemont C, Vieira C: Comparative analysis of transposable elements in the melanogaster subgroup sequenced genomes. Gene 2011, 473:100-109.
• [43]de Lucca M, Carareto C, Ceron C: Distribution of the Bari-I transposable element in stable hybrid strains between Drosophila melanogaster and Drosophila simulans and in Brazilian populations of these species. Genetics and Molecular Biology 2007, 30:676-680.
• [44]Sperlich D: Hybrids between Drosophila melanogaster and D. simulans in nature. Drosophila Information Service 1962, 36:118.
• [45]Yang HP, Hung TL, You TL, Yang TH: Genomewide comparative analysis of the highly abundant transposable element DINE-1 suggests a recent transpositional burst in Drosophila yakuba. Genetics 2006, 173:189-196.
• [46]Heredia F, Loreto ELS, Valente VLS: Complex evolution of gypsy in drosophilid species. Mol Biol Evol 2004, 21:1831-1842.
• [47]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [48]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
• [49]Open Reading Frame Finder. http://www.ncbi.nlm.nih.gov/gorf/gorf.html webcite
• [50]Kimura M: A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 1980, 16:111-120.
• [51]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [52]Bandelt H, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
• [53]Jowett T: Preparation of nucleic acids. In In Drosophila: A Practical Approach. Edited by Roberts DB. Oxford: IRL Press; 1986:275-285.