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The dynamic Eukaryote Genome: Evolution, mobile DNA, and the TE-Thrust hypothesis

Oliver, Keith (2012) The dynamic Eukaryote Genome: Evolution, mobile DNA, and the TE-Thrust hypothesis. PhD thesis, Murdoch University.

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The discovery of transposable elements (TEs) by Barbara McClintock in the 1940s, triggered a new dawning in the development of evolutionary theory. However, similar to Gregor Mendel’s development of the laws of heredity in the nineteenth century, it was a long time before the full significance of this discovery was appreciated. Nevertheless, by the beginning of the 21st century, the study and recognition of TEs as significant factors in evolution was well underway. However, many evolutionary biologists still choose to ignore them, to highlight the loss of fitness in some individuals caused by TEs, or concentrate on the supposed parasitic nature of TEs, and the diseases they cause.

The major concept and theme of this thesis is that the ubiquitous and extremely ancient transposable elements are not merely “junk DNA” or “selfish parasites” but are instead ‘powerful facilitators of evolution’. They can create genomic dynamism, and cause genetic changes of great magnitude and variety in the genotypes and phenotypes of eukaryotic lineages.

A large variety of data are presented supporting the theme of TEs as very significant forces in evolution. This concept is formalised into a hypothesis, the TE-Thrust hypothesis, which explicitly presents detail of how TEs can facilitate evolution. This hypothesis opens the way to explaining otherwise inexplicable aspects of evolution, such as the mismatch between the phyletic gradualism theory, and the punctuated equilibrium concept, which is based on the fossil record.

Data from the studies of many metazoans are analysed, with a focus on the well studied mammals, especially the primates. Data from the seed plants are also included, with a strong focus on Darwin’s ‘abominable mystery’, the rapid origin, and the extraordinary success of the flowering plants.

TEs are ubiquitous and many of them are extremely ancient, probably dating back to the origin of the eukaryotes, and some are also found in prokaryotes. TEs can build, sculpt and reformat genomes by both active and passive means. Active TE-Thrust is due to transpositions by members of the TE consortium, or their retrotransposition of retrocopy genes, or by new acquisitions of TEs, or by the endogenisation of retroviruses, and other similar phenomena. Major results of this are that the promoters carried by TEs can result in very significant alterations in gene expression, and that sequences from the TEs themselves can become exapted or domesticated as novel genes. TEs can also cause exon shuffling, possibly building novel genes. Passive TE-Thrust is due to large homogenous consortia of inactive TEs that can act passively by causing ectopic recombination, resulting in genomic deletions, duplications, and possibly karyotypic changes. TE-Thrust often works together with other facilitators of evolution, such as point mutations, which can occur in duplicated, or retrocopy genes, sometimes resulting in new functions for such genes.

A major concept in the TE-Thrust hypothesis is that although TEs are sometimes harmful to individuals, and can lower the fitness of a population, they endow the lineage of that population with adaptive potential and evolutionary potential. These are extremes of a continuum of intra-genomic potential, and are not separate entities. This adaptive/evolutionary potential due to the presence and activities of the TE consortium of the genomes in a lineage, greatly enhance the future survival prospects of the lineage, and its ability to undergo evolutionary transitions, and/or to radiate into a clade of multiple divergent lineages. Lineages may acquire a TE consortium by new infiltrations of TEs, either by horizontal transposon transfer, de novo synthesis, or endogenisation of retroviruses. Lineages lacking an effective TE consortium are likely to lack adaptive/evolutionary potential and could fail to diversify, become “living fossils”, or even become extinct, as many lineages ultimately do.

The opposite of extinction is the fecund radiation of lineages, and it is shown here that fecund species-rich lineages such as rodents (Order Rodentia) and bats (Order Chiroptera) and the angiosperms, are all well endowed with many viable active TEs. The Simian Primates which have undergone major evolutionary transitions are also well endowed with viable and periodically active TEs, and/or large homogenous populations of TEs. Data on the “living fossils” such as the coelacanth and the tuatara are very limited, but indicate a lack of new acquisitions of TEs, and/or the mutational decay of ancient TE families in their genomes.

Lineages are often in stasis, but a new acquisition of TEs, or other factors such as stress, hybridisation, or whole genome duplications (especially in angiosperms) may trigger a major burst of activity in the TE consortium, resulting in an evolutionary punctuation event. The TE-Thrust hypothesis thus offers an explanation for the punctuated equilibrium, frequently observed in the fossil record.

There are many other known facilitators of evolution, such as point mutations, whole genome duplications, changes in allele frequency, epigenetic changes, symbiosis, hybridisation, simple sequence repeats, karyotypic changes, drift in small populations, allopatric and sympatric reproductive isolation, co-evolution, environmental and ecological changes, and so on. In addition, there may be some as yet unknown facilitators of evolution. However, TEs usually make up between 20 to 80 percent of the genomes of eukaryotes, as against one or two percent of coding genes, and are known to be able to make genomic modifications (“mutations”) that cannot be made by other facilitators of evolution. TEs also come in many superfamilies, and in thousands of families, which make up the mobile DNA of the earth’s biota. It is apparent then that their influence on, and facilitation of, eukaryotic evolution has been very significant indeed. In this thesis data are presented, which indicate that these ubiquitous and extremely ancient TEs are powerful facilitators of change, essential to the evolution of the earth’s biota.

The TE-Thrust hypothesis, when fully explored, developed, and tested, if confirmed, must result in an extension to the Modern Synthesis, or even become a part of a new paradigm of evolutionary theory.

Item Type: Thesis (PhD)
Murdoch Affiliation(s): School of Biological Sciences and Biotechnology
Supervisor(s): McComb, Jen, Greene, Wayne, Tapper, A. and Bradley, Stuart
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