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Review
. 2014 Mar;101(3):163-86.
doi: 10.1007/s00114-014-1152-8. Epub 2014 Feb 4.

The Telomeric Sync Model of Speciation: Species-Wide Telomere Erosion Triggers Cycles of Transposon-Mediated Genomic Rearrangements, Which Underlie the Saltatory Appearance of Nonadaptive Characters

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Review

The Telomeric Sync Model of Speciation: Species-Wide Telomere Erosion Triggers Cycles of Transposon-Mediated Genomic Rearrangements, Which Underlie the Saltatory Appearance of Nonadaptive Characters

Reinhard Stindl. Naturwissenschaften. .
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Abstract

Charles Darwin knew that the fossil record is not overwhelmingly supportive of genetic and phenotypic gradualism; therefore, he developed the core of his theory on the basis of breeding experiments. Here, I present evidence for the existence of a cell biological mechanism that strongly points to the almost forgotten European concept of saltatory evolution of nonadaptive characters, which is in perfect agreement with the gaps in the fossil record. The standard model of chromosomal evolution has always been handicapped by a paradox, namely, how speciation can occur by spontaneous chromosomal rearrangements that are known to decrease the fertility of heterozygotes in a population. However, the hallmark of almost all closely related species is a differing chromosome complement and therefore chromosomal rearrangements seem to be crucial for speciation. Telomeres, the caps of eukaryotic chromosomes, erode in somatic tissues during life, but have been thought to remain stable in the germline of a species. Recently, a large human study spanning three healthy generations clearly found a cumulative telomere effect, which is indicative of transgenerational telomere erosion in the human species. The telomeric sync model of speciation presented here is based on telomere erosion between generations, which leads to identical fusions of chromosomes and triggers a transposon-mediated genomic repatterning in the germline of many individuals of a species. The phenotypic outcome of the telomere-triggered transposon activity is the saltatory appearance of nonadaptive characters simultaneously in many individuals. Transgenerational telomere erosion is therefore the material basis of aging at the species level.

Figures

Fig. 1
Fig. 1
Schindewolf’s typostrophic theory as published in 1950 (Schindewolf , p. 202). During the short typogenetic phase, the type breaks up into subtypes with new body plans. The lengthy typostatic phase is characterized by phenotypes, which remain rather stable with only smooth and gradual transformations. In the brief, final typolytic phase, these subtypes produce all kinds of degenerative offshoots. During the typostatic phase, evolutionary cycles of lesser rank branch off and during their typostatic phase other branches appear that go through typogenesis, typostasis and typolysis, and so on. (Figure adapted from Schindewolf 1993)
Fig. 2
Fig. 2
How many bottlenecks are required to generate this kind of karyotypical mess between closely related species? a Gibbon (Hylobates lar) karyotype in comparison to b human karyotype based on corresponding color code. Every sporadic chromosomal aberration reduces fertility of heterozygotes due to loss of genetically unbalanced offspring. So how could fixation of these massively reorganized karyotypes ever occur based on standard models (Jauch et al. 1992)? Fluorescence in situ hybridization was performed on metaphase chromosomes of a male gibbon and a male human with human multicolor FISH probes from Metasystems according to the suppliers protocol except for a slightly reduced temperature at the post-hybridization wash for the gibbon. (Unpublished result of a hybridization experiment performed by the author at the University of California at Berkeley in January 2002. The gibbon cell line was kindly provided by Johannes Wienberg at the Institute of Human Genetics at the Ludwig-Maximilians University in Munich and by Christa Lese Martin and Lorraine May at the Department of Human Genetics at the University of Chicago)
Fig. 3
Fig. 3
Telomeres are the protective caps at the ends of eukaryotic chromosomes. Telomeres (red) on human chromosomes (blue). PNA-FISH was performed by the author, according to standard protocols (Daco) at the Medical University of Vienna in 2006
Fig. 4
Fig. 4
The theoretical concept of transgenerational telomere erosion in the female germline with a carry-over effect for both sexes is in perfect agreement with published data of large multigenerational studies on healthy individuals. Contrary to the mainstream view of a significant telomere length increase in the testes of very old men, I suggest that the old-father-long-telomered-offspring effect (Eisenberg et al. 2012) strongly point to ever-shortening telomeres in the female germline. According to my interpretation, telomerase basically stabilizes telomeres in testes and, therefore, the offspring of old fathers bypass the telomere loss of one female generation (figure reprinted from Stindl 2011). Very old fathers tend to have younger wives (because of social and biological reasons), whereas older mothers usually have husbands of similar advanced age, possibly resulting in a reduced loss of their offspring’s telomere length. Therefore, the negative age effect of older mothers on their offspring’s telomeres was only found in one large study, where the authors carefully adjusted for paternal age at conception (Prescott et al. 2012)
Fig. 5
Fig. 5
The telomeric sync model of speciation and Schindewolf’s three phases of typostrophic theory exemplified by the widespread centric fusion–fission cycle of acrocentric chromosomes. a Typogenesis: after the splitting of metacentric chromosomes in the typolytic phase, telomeres are rebuilt and lengthened at the beginning of the typogenetic phase. The high frequency of eroded telomeres at the transition phase between typolysis and typogenesis triggers a massive transposon-mediated repatterning of the genome that explosively creates the new body plans of new species during typogenesis. b Typostasis: transgenerational telomere erosion leads to the sequential fusions of acrocentric chromosomes with only limited transposon-mediated genomic repatterning. Consequently, new species with only minor phenotypic adaptations occur. This phase is characterized by a more gradual pattern of evolution proceeding in an orthogenetic direction. An example for the limited phenotypic change is the transition from the Przewalski to the domestic horse (Yang et al. 2003). c Typolysis: at the end of the line, once all acrocentric chromosomes fused and became metacentric chromosomes, the lineage either undergoes a massive splitting of metacentric chromosomes and starts again or dies from chromosomal instability. Eroded telomeres on many chromosomes lead to a burst of transposon activity. According to the fossil record, pseudovariability and degenerative diseases characterize species phenotypes, shortly before their complete disappearance. During the lengthy typostatic phase, eventually new evolutionary cycles branch off due to the combination of chromosomal aberrations and significant transposon-mediated genomic repatterning
Fig. 6
Fig. 6
Centric fusion–fission cycle in combination with pericentric inversions as the theoretical model for rearranged karyotypes as seen in gibbons compared to humans. In contrast to current mainstream models, no translocations between different chromosomes are required, which bear a higher risk for unbalanced offspring

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