Extreme Telomere Length Dimorphism in the Tasmanian Devil and Related Marsupials Suggests Parental Control of Telomere Length

Abstract

Telomeres, specialised structures that protect chromosome ends, play a critical role in preserving chromosome integrity. Telomere dynamics in the Tasmanian devil (Sarcophilus harrisii) are of particular interest in light of the emergence of devil facial tumour disease (DFTD), a transmissible malignancy that causes rapid mortality and threatens the species with extinction. We used fluorescent in situ hybridisation to investigate telomere length in DFTD cells, in healthy Tasmanian devils and in four closely related marsupial species. Here we report that animals in the Order Dasyuromorphia have chromosomes characterised by striking telomere length dimorphism between homologues. Findings in sex chromosomes suggest that telomere length dimorphism may be regulated by events in the parental germlines. Long telomeres on the Y chromosome imply that telomere lengthening occurs during spermatogenesis, whereas telomere diminution occurs during oogenesis. Although found in several somatic cell tissue types, telomere length dimorphism was not found in DFTD cancer cells, which are characterised by uniformly short telomeres. This is, to our knowledge, the first report of naturally occurring telomere length dimorphism in any species and suggests a novel strategy of telomere length control. Comparative studies in five distantly related marsupials and a monotreme indicate that telomere dimorphism evolved at least 50 million years ago.

Telomere Length and Genetic Anticipation in Lynch Syndrome

“…Although the sample size of parent-child pairs is very limited, this observation might suggest that the maternally transmitted risk mechanism is shortened telomeres. Studies assessing whether telomere shortening occurs in the female germline, as recently demonstrated in other mammals [37], together with the analysis of larger samples of LS parent-child pairs, are required to verify this hypothesis.…”

Evolutionary ecology of telomeres: a review

“…Barrett and Richardson also provide an insightful discussion of potential genetic mechanisms explaining among‐taxa differences in telomere dynamics (such as the role of heterogamety), but data are (in our opinion) too meager to provide a general theory. Interestingly, in the marsupial Tasmanian devil ( Sarcophilus harrisii ), telomeres are strikingly dimorphic between homologues, with a lengthening process during spermatogenesis (on the Y chromosome) and a shortening process during oogenesis . Furthermore, the Tasmanian devil is fraught with one of the few described contagious cancers in wild populations, and the tumors resulting from transfer of the malignant cells during agonistic interactions all have characteristically short telomeres …”

“…Interestingly, in the marsupial Tasmanian devil (Sarcophilus harrisii), telomeres are strikingly dimorphic between homologues, with a lengthening process during spermatogenesis (on the Y chromosome) and a shortening process during oogenesis. 70 Furthermore, the Tasmanian devil is fraught with one of the few described contagious cancers in wild populations, and the tumors resulting from transfer of the malignant cells during agonistic interactions all have characteristically short telomeres. 70 Few species have been examined in which males' and females' life history strategies and associated reproductive investments are drastically different.…”

“…70 Furthermore, the Tasmanian devil is fraught with one of the few described contagious cancers in wild populations, and the tumors resulting from transfer of the malignant cells during agonistic interactions all have characteristically short telomeres. 70 Few species have been examined in which males' and females' life history strategies and associated reproductive investments are drastically different. One such case, however, is the red-sided garter snake (Thamnophis sirtalis parietalis), 14 in which males and females differ in their corticosterone levels (higher in males) following hibernation and males engage in mate searching, courtship, and mating behavior, whereas females have a more passive role.…”

Kangaroo gene mapping and sequencing: insights into mammalian genome evolution

“…Dasyurid telomeres have recently been found to exhibit a parent-specific control of length (Bender et al 2012). This was first observed in Tasmanian devils as extremely heterogeneous binding of telomere-specific sequences to the two homologues of each chromosome: one haploid set had small telomeres, and the other set had enormous telomeres.…”