Abstract
Telomeres are protective structures at the ends of eukaryotic chromosomes, and disruption of their nucleoprotein composition usually results in genome instability and cell death. Telomeric DNA sequences have generally been found to be exceptionally conserved in evolution, and the most common pattern of telomeric sequences across eukaryotes is (TxAyGz)n maintained by telomerase. However, telomerase-added DNA repeats in some insect taxa frequently vary, show unusual features, and can even be absent. It has been speculated about factors that might allow frequent changes in telomere composition in Insecta. Coleoptera (beetles) is the largest of all insect orders and based on previously available data, it seemed that the telomeric sequence of beetles varies to a great extent. We performed an extensive mapping of the (TTAGG)n sequence, the ancestral telomeric sequence in Insects, across the main branches of Coleoptera. Our study indicates that the (TTAGG)n sequence has been repeatedly or completely lost in more than half of the tested beetle superfamilies. Although the exact telomeric motif in most of the (TTAGG)n-negative beetles is unknown, we found that the (TTAGG)n sequence has been replaced by two alternative telomeric motifs, the (TCAGG)n and (TTAGGG)n, in at least three superfamilies of Coleoptera. The diversity of the telomeric motifs was positively related to the species richness of taxa, regardless of the age of the taxa. The presence/absence of the (TTAGG)n sequence highly varied within the Curculionoidea, Chrysomeloidea, and Staphylinoidea, which are the three most diverse superfamilies within Metazoa. Our data supports the hypothesis that telomere dysfunctions can initiate rapid genomic changes that lead to reproductive isolation and speciation.
Highlights
Telomeres are protective structures at the ends of eukaryotic chromosomes, and disruption of their nucleoprotein composition usually results in genome instability and cell death
The (TTAGG)n sequence is considered the ancestral telomeric motif of arthropods, the sequence has been lost in numerous insect orders[11,12]
The goal of our study was to understand the high rate of change in beetle telomere sequences via an extensive mapping of (TTAGG)n and (TCAGG)n telomeric sequences across the main branches of the order, a dramatic increase in species sampling compared to existing studies, identification of novel telomeric repeats, and interpretation of our data with the recently determined phylogenetic relationships, species richness and age of the tested clades
Summary
Telomeres are protective structures at the ends of eukaryotic chromosomes, and disruption of their nucleoprotein composition usually results in genome instability and cell death. Telomere length is most often maintained by a specialized RNA-dependent DNA polymerase called telomerase, which anneals to the 3′ end of chromosomes and repeatedly attaches short non-coding tandem sequences, usually 5–8-bp long, using its internal RNA subunit as a template. The activity of this enzyme is highly regulated and is generally associated with proliferating cells, such as embryonic or germ cells, while activity is low in quiescent, differentiated c ells[2,3]. There are taxa in which telomerase-added DNA repeats frequently vary, show unusual features, or have been lost and replaced by a completely different mechanism of telomere loss compensation. With 155,477 species[18], Diptera is a highly successful order among insects, which shows that the loss of telomerase is not a limiting factor for insect evolution and leads us to a question how widespread non-telomerase systems and the insect telomeric motif are among insects[7]
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