SINEs of speciation: tracking lineages with retroposons.

The value of short interspersed elements (SINEs) for diagnosing common ancestry is being expanded to examine the differential sorting of lineages through the course of speciation events. Because most SINEs are neutral markers of identical descent, are not precisely excised from the genome and have a known ancestral condition, they are advantageous for reconciling gene trees and species trees with minimal phylogenetic error. A population perspective on SINE evolution combined with coalescence theory provides a context for investigating the phenomenon of ancestral polymorphism and its role in producing incongruent SINE insertion patterns among multiple loci. Studies of human Alu repeats demonstrate the value of young polymorphic SINEs for assessing human genomic diversity and tracking ancient demographics of human populations, whereas incongruent insertion patterns revealed by older fixed SINE loci, such as those in African cichlid fishes, contain information that might help identify ancient radiations that are otherwise obscured by accumulated mutations in sequence data. Here, we review the utility of retroposons for inferring common ancestry, discuss limits to the method, and clarify confusion by providing examples from the literature that illustrate how discordant multi-locus insertion patterns of retroelements can indicate lineage-sorting events that should not be misinterpreted as phylogenetic noise.

[1]  P. Donnelly,et al.  Alu insertion polymorphisms in humans: A review , 2001 .

[2]  N Okada,et al.  SINE evolution, missing data, and the origin of whales. , 2000, Systematic biology.

[3]  Nancy F. Hansen,et al.  Comparative analyses of multi-species sequences from targeted genomic regions , 2003, Nature.

[4]  R. Gibbs,et al.  A human dimorphism resulting from loss of an Alu. , 1992, Genomics.

[5]  T. Kocher.  Adaptive evolution and explosive speciation: the cichlid fish model , 2004, Nature Reviews Genetics.

[6]  M. Batzer,et al.  Alu elements and hominid phylogenetics , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A. Meyer,et al.  Total evidence: molecules, morphology, and the phylogenetics of cichlid fishes. , 2000, The Journal of experimental zoology.

[8]  A. Smit.  Interspersed repeats and other mementos of transposable elements in mammalian genomes. , 1999, Current opinion in genetics & development.

[9]  J. Brosius,et al.  Retroposons--seeds of evolution. , 1991, Science.

[10]  Jerilyn A. Walker,et al.  Following the LINEs: an analysis of primate genomic variation at human-specific LINE-1 insertion sites. , 2003, Molecular biology and evolution.

[11]  P. Holland,et al.  Rare genomic changes as a tool for phylogenetics. , 2000, Trends in ecology & evolution.

[12]  M. Batzer,et al.  Non-traditional Alu evolution and primate genomic diversity. , 2002, Journal of molecular biology.

[13]  N. Okada,et al.  Determination of the phylogenetic relationships among Pacific salmonids by using short interspersed elements (SINEs) as temporal landmarks of evolution. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. Nishida,et al.  Retroposition of the AFC Family of SINEs (Short Interspersed Repetitive Elements) Before and During the Adaptive Radiation of Cichlid Fishes in Lake Malawi and Related Inferences About Phylogeny , 2001, Journal of Molecular Evolution.

[15]  C. Schmid,et al.  Does SINE evolution preclude Alu function? , 1998, Nucleic acids research.

[16]  S. Sherry,et al.  Alu evolution in human populations: using the coalescent to estimate effective population size. , 1997, Genetics.

[17]  R. Britten,et al.  Mobile elements inserted in the distant past have taken on important functions. , 1997, Gene.

[18]  R. J. Herrera,et al.  African origin of human-specific polymorphic Alu insertions. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Batzer,et al.  Potential gene conversion and source genes for recently integrated Alu elements. , 2000, Genome research.

[20]  M. Stoneking,et al.  Mitochondrial DNA and human evolution , 1987, Nature.

[21]  DETECTING CORRELATION BETWEEN CHARACTERS IN A COMPARATIVE ANALYSIS WITH UNCERTAIN PHYLOGENY , 2003, Evolution; international journal of organic evolution.

[22]  A. Meyer,et al.  The Cytochrome b Gene as a Phylogenetic Marker: The Limits of Resolution for Analyzing Relationships Among Cichlid Fishes , 2001, Journal of Molecular Evolution.

[23]  N. Okada,et al.  Molecular evidence from retroposons that whales form a clade within even-toed ungulates , 1997, Nature.

[24]  M. Stoneking,et al.  Alu insertion polymorphisms and human evolution: evidence for a larger population size in Africa. , 1997, Genome research.

[25]  N. Takahata.  Gene genealogy in three related populations: consistency probability between gene and population trees. , 1989, Genetics.

[26]  M. Batzer,et al.  Recently integrated Alu elements and human genomic diversity. , 2003, Molecular biology and evolution.

[27]  J. Klein,et al.  Persistence of neutral polymorphisms in Lake Victoria cichlid fish. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Nishida,et al.  Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposons. , 2001, Molecular biology and evolution.

[29]  Mouse Genome Sequencing Consortium.  Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[30]  H. Endoh,et al.  Total DNA transcription in vitro: a procedure to detect highly repetitive and transcribable sequences with tRNA-like structures. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Nishida,et al.  A novel family of short interspersed repetitive elements (SINEs) from cichlids: the patterns of insertion of SINEs at orthologous loci support the proposed monophyly of four major groups of cichlid fishes in Lake Tanganyika. , 1998, Molecular biology and evolution.

[32]  M. Hasegawa,et al.  Retroposon analysis of major cetacean lineages: The monophyly of toothed whales and the paraphyly of river dolphins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  A. Weiner.  SINEs and LINEs: the art of biting the hand that feeds you. , 2002, Current opinion in cell biology.

[34]  M. Batzer,et al.  Alu repeats and human genomic diversity , 2002, Nature Reviews Genetics.

[35]  M. Batzer,et al.  Alu insertion polymorphisms for the study of human genomic diversity. , 2001, Genetics.

[36]  L. Cavalli-Sforza,et al.  High resolution of human evolutionary trees with polymorphic microsatellites , 1994, Nature.

[37]  M. Kimura,et al.  The neutral theory of molecular evolution. , 1983, Scientific American.

[38]  R. Maraia,et al.  The impact of short interspersed elements (SINEs) on the host genome , 1995 .

[39]  D. Hillis,et al.  SINEs of the perfect character. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Batzer,et al.  A human-specific subfamily of Alu sequences. , 1991, Genomics.

[41]  S T Sherry,et al.  Genetic traces of ancient demography. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[42]  I. Kornfield,et al.  Retention of an ancestral polymorphism in the Mbuna species flock (Teleostei: Cichlidae) of Lake Malawi , 1993 .

[43]  J. Avise.  Phylogeography: The History and Formation of Species , 2000 .

[44]  N Okada,et al.  Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Ziheng Yang,et al.  Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. , 2003, Genetics.

[46]  H. Kazazian.  Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[47]  K. Olsson,et al.  An ancient retrovirus-like element contains hot spots for SINE insertion. , 2001, Genetics.

[48]  A. Meyer,et al.  Response to Comment on "Origin of the Superflock of Cichlid Fishes from Lake Victoria, East Africa" , 2004, Science.

[49]  Jerilyn A. Walker,et al.  Genetic variation among world populations: inferences from 100 Alu insertion polymorphisms. , 2003, Genome research.

[50]  J. Klein,et al.  Phylogenetic Relationships Among East African Haplochromine Fish as Revealed by Short Interspersed Elements (SINEs) , 2003, Journal of Molecular Evolution.

[51]  M. Batzer,et al.  Evolution of Retroposons , 1993 .

[52]  J. Schmitz,et al.  The colugo (Cynocephalus variegatus, Dermoptera): the primates' gliding sister? , 2002, Molecular biology and evolution.

[53]  B. Rannala,et al.  DETECTING CORRELATION BETWEEN CHARACTERS IN A COMPARATIVE ANALYSIS WITH UNCERTAIN PHYLOGENY , 2003, Evolution; international journal of organic evolution.

[54]  T. Kocher.  Evolutionary biology: Fractious phylogenies , 2003, Nature.

[55]  H H Kazazian,et al.  HUGO—a midlife crisis? , 1998, Nature Genetics.

[56]  N. Okada,et al.  Retroposon mapping in molecular systematics. , 2004, Methods in molecular biology.

[57]  J. V. Moran,et al.  Initial sequencing and analysis of the human genome. , 2001, Nature.

[58]  M. Milinkovitch,et al.  Evolutionary biology: Even-toed fingerprints on whale ancestry , 1997, Nature.

[59]  G. Turner,et al.  Extensive homoplasy, nonstepwise mutations, and shared ancestral polymorphism at a complex microsatellite locus in Lake Malawi cichlids. , 2000, Molecular biology and evolution.

[60]  N Okada,et al.  SINE insertions: powerful tools for molecular systematics. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[61]  M. Nei.  Molecular Evolutionary Genetics , 1987 .

[62]  M. Nei,et al.  Molecular Evolution and Phylogenetics , 2000 .

[63]  Michael F. Hammer,et al.  A recent common ancestry for human Y chromosomes , 1995, Nature.

[64]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[65]  M. Nishida,et al.  Using SINEs to probe ancient explosive speciation: "hidden" radiation of African cichlids? , 2003, Molecular biology and evolution.

[66]  N. Okada,et al.  Detection of the ongoing sorting of ancestrally polymorphic SINEs toward fixation or loss in populations of two species of charr during speciation. , 1998, Genetics.

[67]  H. Tachida,et al.  A population genetic study of the evolution of SINEs. I. Polymorphism with regard to the presence or absence of an element. , 1993, Genetics.