Are the TTAGG and TTAGGG telomeric repeats phylogenetically conserved in aculeate Hymenoptera?

Abstract

Despite the (TTAGG) telomeric repeat supposed being the ancestral DNA motif of telomeres in insects, it was repeatedly lost within some insect orders. Notably, parasitoid hymenopterans and the social wasp Metapolybia decorata (Gribodo) lack the (TTAGG) sequence, but in other representatives of Hymenoptera, this motif was noticed, such as different ant species and the honeybee. These findings raise the question of whether the insect telomeric repeat is or not phylogenetically predominant in Hymenoptera. Thus, we evaluated the occurrence of both the (TTAGG) sequence and the vertebrate telomere sequence (TTAGGG) using dot-blotting hybridization in 25 aculeate species of Hymenoptera. Our results revealed the absence of (TTAGG) sequence in all tested species, elevating the number of hymenopteran families lacking this telomeric sequence to 13 out of the 15 tested families so far. The (TTAGGG) was not observed in any tested species. Based on our data and compiled information, we suggest that the (TTAGG) sequence was putatively lost in the ancestor of Apocrita with at least two subsequent independent regains (in Formicidae and Apidae).

Telomere structure in insects: A review

“…A few years later, Gokhman et al () also showed absence of this repeat in several superfamilies of parasitoid Hymenoptera including Chalcidoidea. Futhermore, Menezes et al () and Menezes et al () have demonstrated absence of the (TTAGG) n motif in most aculeate Hymenoptera and independent reappearance of this repeat in the families Formicidae and Apidae. Nevertheless, in contrast to Apocrita (=Parasitica + Aculeata), presence of the TTAGG telomeric repeat in the only other existing suborder of this group, i.e., Symphyta, was not investigated until the last years.…”

“…On the other hand, Odonata could initially lack the TTAGG telomeric sequence. If this is true, the (TTAGG) n motif independently reappears in S. vulgatum (Kuznetsova et al, ); an analogous situation occurs, e.g., in aculeate Hymenoptera (see Menezes et al, ). An alternative explanation is that this repeat represents a persisting but non‐functional relict of the ancestral telomeric motif/subtelomeric region, as suggested by Korandová et al () for similar cases.…”

“…Coexistence of different (either active or disabled) mechanisms of telomere replication in most insects can therefore explain losses and reappearances of the TTAGG repeat in insect evolution, including an apparent absence of this motif in Antliophora as well as the change of this repeat to TCAGG in certain clades of the order Coleoptera. In addition, a few higher taxa, e.g., Heteroptera (Hemiptera) and Hymenoptera, show presence of the (TTAGG) n motif in their basal clades as well as a subsequent loss and, at least in the Hymenoptera, independent reappearance of this motif in some advanced groups (Angus et al, ; Chirino et al, ; Gokhman & Kuznetsova, ; Menezes et al, ; Pita et al, ). This also shows the importance of phylogenetic inference for reconstructing evolutionary transformations of telomere structure.…”

“…Recent research on insect telomeres has revealed several examples of heterogeneity for presence/absence of the (TTAGG) n motif within, e.g., Hemiptera: Heteroptera (Angus, Jeangirard, Stoianova, Grozeva, & Kuznetsova, ; Chirino, Dalíková, Marec, & Bressa, ; Golub, Golub, & Kuznetsova, , , ; Grozeva, Kuznetsova, & Anokhin, ; Kuznetsova, Grozeva, & Anokhin, ; Pita et al, ) and Hymenoptera (Gokhman, Anokhin, & Kuznetsova, ; Gokhman & Kuznetsova, ; Menezes, Bardella, Cabral‐de‐Mello, Lucena, & Almeida, ; Menezes et al, ), and even between closely related species of the order Odonata (Kuznetsova, Maryańska‐Nadachowska, Shapoval, Anokhin, & Shapoval, ). Insects that lack canonical telomeric repeats probably constitute about 10%–15% of all animal species (Mason et al, ).…”

“…Since this compilation, the number of species and higher taxa targeted by telomere studies experienced a manifold increase. New data became available for many previously poorly studied or unexplored orders such as Odonata (Kuznetsova et al, ), Orthoptera (Buleu, Jetybayev, Chobanov, & Bugrov, ; Kociński, Grzywacz, Chobanov, & Warchałowska‐Śliwa, ), Phasmatodea (Liehr, Buleu, Karamysheva, Bugrov, & Rubtsov, ; Scali et al, ), Mantophasmatodea (Lachowska‐Cierlik, Maryańska‐Nadachowska, Kuznetsova, & Picker, ), Hemiptera (Anjos, Rocha, Paladini, Mariguela, & Cabral‐de‐Mello, ; Chirino et al, ; Grozeva, Kuznetsova, & Anokhin, ; Kuznetsova, Grozeva, Hartung, & Anokhin, ; Luan, Sun, Fei, & Douglas, ; Mandrioli, Zanasi, & Manicardi, ; Maryańska‐Nadachowska, Kuznetsova, Golub, & Anokhin, ; Mohan, Rani, Kulashreshta, & Kadandale, ), Neuroptera (Kuznetsova, Khabiev, & Anokhin, ), Coleoptera (Mravinac et al, ), Hymenoptera (Gokhman et al, ; Gokhman & Kuznetsova, ; Menezes et al, ) and others (see Figure , Appendix ). All this information was mainly obtained by FISH and is therefore more reliable if compared with SBH, because, when (TTAGG) n sequences are detected by the latter technique, they are not necessarily telomeric, as the specific probe could also hybridize with repetitive sequences located at non‐telomeric sites (Meyne et al, ; Sahara et al, ).…”