Mobile DNA and the TE-Thrust hypothesis: supporting evidence from the primates

Abstract

Transposable elements (TEs) are increasingly being recognized as powerful facilitators of evolution. We propose the TE-Thrust hypothesis to encompass TE-facilitated processes by which genomes self-engineer coding, regulatory, karyotypic or other genetic changes. Although TEs are occasionally harmful to some individuals, genomic dynamism caused by TEs can be very beneficial to lineages. This can result in differential survival and differential fecundity of lineages. Lineages with an abundant and suitable repertoire of TEs have enhanced evolutionary potential and, if all else is equal, tend to be fecund, resulting in species-rich adaptive radiations, and/or they tend to undergo major evolutionary transitions. Many other mechanisms of genomic change are also important in evolution, and whether the evolutionary potential of TE-Thrust is realized is heavily dependent on environmental and ecological factors. The large contribution of TEs to evolutionary innovation is particularly well documented in the primate lineage. In this paper, we review numerous cases of beneficial TE-caused modifications to the genomes of higher primates, which strongly support our TE-Thrust hypothesis.

Potential impact of primate-specific SVA retrotransposons during the evolution of human cognitive function

“…4,16 SVAs can also induce alternative splicing and exon skipping which can result in the generation of alternative transcripts of a gene as documented by disease causing insertions. [17][18][19] Thus SVA insertions may generate new interactions between what would otherwise be distinct pathways.…”

“…4,5 The large number of such TEs in the genome makes an analysis of their specific contribution to evolution very difficult, and previous studies highlighted the potential role of mainly self-propagating (L1, ERV/ETR) and Alu elements. 4 We have focused on the functions of genes in proximity to the integration sites of the less studied hominoid-specific composite retrotransposons termed SINE-VNTR-Alu (SVA) elements. 6 SVA elements represent the youngest non-LTR retrotransposon family in humans and the human genome harbors approximately 2700 SVAs.…”

“…Transposable elements (TEs), despite long being thought of as junk DNA, have impacted the human genome during its evolution through a variety of mechanisms causing structural variations including insertional mutagenesis, generation of deletions at the insertion site, 3' or 5' transduction events, non-allelic homologous recombination and exonisation. [1][2][3][4] More than 10,000 TE insertions occurred in the human genome since human-chimpanzee divergence which were suggested to have implications on human evolution and especially its reproductive, cognitive and immune functions that diverged strongly during a relative short time period. 4,5 The large number of such TEs in the genome makes an analysis of their specific contribution to evolution very difficult, and previous studies highlighted the potential role of mainly self-propagating (L1, ERV/ETR) and Alu elements.…”

“…[1][2][3][4] More than 10,000 TE insertions occurred in the human genome since human-chimpanzee divergence which were suggested to have implications on human evolution and especially its reproductive, cognitive and immune functions that diverged strongly during a relative short time period. 4,5 The large number of such TEs in the genome makes an analysis of their specific contribution to evolution very difficult, and previous studies highlighted the potential role of mainly self-propagating (L1, ERV/ETR) and Alu elements. 4 We have focused on the functions of genes in proximity to the integration sites of the less studied hominoid-specific composite retrotransposons termed SINE-VNTR-Alu (SVA) elements.…”

“…8 Therefore, SVA insertions established in the hominoid lineage could be responsible for altering the transcriptome in a developmental, tissue-specific or stimulus inducible manner, as was already suggested earlier for Alu elements and demonstrated for LTR sequences of endogenous retroviruses. 4 SVA elements are categorized into subfamilies A to F and F1, 11 and their age was estimated at 13.56 million years (Myrs) for the oldest subfamily (A) and 3.18 Myrs for the youngest subfamily (F). Subfamily D is by far the largest and encompasses 44% of all SVAs in the human genome.…”