Is telomere erosion a mechanism of species extinction?

Abstract

According to the fossil record, 99.9% of all species that have ever lived on Earth have disappeared. However, only about 4% died out during the five mass extinction events, whereas it seems that the majority of species vanished without any signs of significant earthbound or extraterrestrial physical threats. Clearly, biological extinction mechanisms are by far the most important, but they are subject to serious limitations concerning the worldwide disappearance of species. In view of that, species-inherent mechanisms, which could lead to the worldwide destabilization of a population, might be worth reconsideration. Telomeres, the protective caps of chromosome ends, and the enzyme telomerase have been well preserved in plants and animals during evolution. In the absence of telomerase activity, telomeric DNA has been shown to shorten every time a cell divides. The concept of a mitotic clock based on the gradual erosion of telomeres is now generally accepted and has been confirmed in numerous plants and animals. Chromosomal rearrangements are the hallmarks of two completely different biological phenomena, cancer and speciation. In premalignant cells, gradual telomere erosion beyond a critical threshold is a well-known inducer of chromosomal instability. The species clock hypothesis, as presented here, is based on the idea of a tiny loss of mean telomere length per generation. This mechanism would not rapidly endanger the survival of a particular species. Yet, after many thousands of generations, critically short telomeres could lead to the weakening and even the extinction of old species and would simultaneously create the unstable chromosomal environment that might result in the origination of new species.

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

“…Although I recommend two of my original papers (Stindl 2004a, 2011) for further study, here I briefly recapitulate the main points. Telomeres are the protective caps of eukaryotic chromosome ends (Fig.…”

“…In 2004, I presented an alternative evolutionary model based on transgenerational telomere erosion and recurrent cycles of chromosomal instability, which result in either chromosomal fusions (and new species) or telomere stabilization or species extinction (Stindl 2004a). The so-called species clock hypothesis is based on the idea that telomere erosion synchronizes speciation events in many individuals, similar to such biological phenomena as the mass flowering events of bamboo, which occur (up to) every 120 years (Janzen 1976).…”

“…3) and it has been shown that critically short telomeres result in chromosomal instability (Londono-Vallejo 2004). Based on the assumption that telomeres shorten between generations (Stindl 2004a) and the fact that certain chromosome arms tend to have the shortest telomeres in a species (Graakjaer et al 2006), it was proposed that the same chromosomal fusion product appears independently in several individuals’ germline, leading to homozygous offspring without the underdominance problem of heterozygotic carriers (Stindl 2004a).

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“…In human male embryos, such an in vivo process has been described exclusively for sex chromosomes (Perner et al 2003), where telomere lengths of the long arms of the X and Y chromosomes appear to become homogenized, possibly due to interchromosomal recombination of subtelomeres. An alternative scenario for the average telomere length of the Y chromosome is that intergenerational telomere erosion proceeds slowly in male and female germlines (Stindl 2004a), and accelerated erosion in one of the two sexes is only a late-stage characteristic of an “aged” species.…”

“…To explain pericentric inversions and other structural chromosomal aberrations (besides fusions of acrocentrics) and the saltatory phenotypic change that occurred during evolution, I realized that it is time for an upgrade of my species clock hypothesis (Stindl 2004a). In the following section, I will present an advanced version, but first comes a survey of the supportive data from the literature.…”