SINEs of speciation: tracking lineages with retroposons

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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.

Section snippets

Detecting and characterizing new SINEs

The step-by-step process of isolating and characterizing new SINEs for systematic studies has been reviewed in detail [40]. To discover new elements, we can take advantage of the fact that most SINEs are derived from tRNAs and thus have a tRNA-like secondary structure as well as internal promoters for RNA polymerase III. If we know which family of SINEs to expect in a host genome, we can experimentally screen a genomic library of a species of interest with an oligonucleotide probe that is

Limits to SINE analysis

A debate over the limits to the SINE approach has scrutinized the nature of how these genetic markers evolve and how frequently exceptional patterns occur. Crucial assumptions of the method are based on the absence of any known precise deletions of SINE elements and the rarity of parallel insertion events at the exact same site in the genomes of different taxa. Apparent cases of parallel SINE insertion in different lineages have been investigated 42, 43, 44. This phenomenon is a rare random

Fixation of SINEs

Most SINEs that insert into nonfunctional regions throughout the genome do not impart any obvious advantage or disadvantage to the host and they are generally considered to be neutral genetic markers. Hence, their evolution among species can be modeled with the use of neutral theory 46, 47. The time to fixation of a SINE under neutral conditions is usually far shorter than the length of time between lineage splits. In this case, the SINE method gives a robust evolutionary tree without concern

Assessing human genomic diversity with SINEs

Not surprisingly, the Human Genome Project has had a major influence on the study of SINEs, which are the most abundant elements in the mobile DNA that accounts for ∼45% of the chromosomes of humans. Alu elements are human- and primate-specific SINEs that have proliferated to more than a million copies in the human genome over the past ∼65 Myr. Through this dynamic process, they have generated a substantial amount of genetic diversity in our species 4, 52. Alu insertions continue to fuel the

Conclusions

SINEs continue to provide both insight into the role that mobile DNA has played in shaping genomes and a wealth of neutral genetic markers of identical descent and known ancestral condition. Limits to the use of SINEs include the decay of PCR priming sites after ∼150–200 Myr and the large effort needed to establish an informative multi-locus data set for many taxa. In particular, the fundamental assumptions of SINE insertion analysis, namely the rarity of parallel insertion events and lack of

Acknowledgements

We thank Joe Felsenstein, Scott Edwards, Peter Beerli, Mary Kuhner, Alan Weiner, Leroy Hood, Arian Smit, Bruce Rannala, Hidenori Tachida, Masatoshi Nei and Masami Hasegawa for helpful discussions and critical comments. Three anonymous referees provided valuable suggestions that improved earlier versions of the article. This review was produced with support from NSF-JSPS international fellowship P98881 to A.M.S. and Monbusho grant-in-aid for special research to N.O. Additional collaborative

Glossary

Ancestral polymorphism:
a situation in which incomplete sorting of gene copies over generations might lead to fixation of alleles in descendant species whose genealogical structure does not reflect the true species phylogeny.
Clade:
a natural taxon originating with a common ancestor and including all descendants; a monophyletic group.
Coalescence theory:
numerical framework that enables one to use various population genetic models to calculate probabilities of genealogical structure among copies of

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