Stability of instability… when karyotype is never the same
Aphids are common insects that reproduce primarily by apomictic parthenogenesis, a form of reproduction whereby adult females give birth to a female progeny without any male fertilization. It has been frequently suggested that in the parthenogenetic generations no genetic recombination occurs, so that it has been assumed that the offspring represents a genetically identical clone of aphids.

Actually, aphid lineages within a same species can differ for colour, size, intrinsic rate of increase, ovariole number, reproductive modes, ability to transfer pathogenic plant viruses and susceptibility/resistance to predators, parasites, pathogens and pesticides strongly suggesting that clonality in aphids have been overestimated.

In the last years a growing amount of molecular evidences suggested that aphid asexual lineages are not true clones, since they can rapidly mutate. Molecular analyses, such as amplified fragment length polymorphism (AFLP), have provided unequivocal evidences of mutational changes due to somatic event recombination. Similarly, microsatellite mutations within apparent clonal lineages have also been reported.

Clone or not? Several papers showed in the peach potato aphid Myzus persicae variations in the chromosome number mainly due to chromosomal translocations and, occasionally, to fragmentations that result in an increased chromosome number. These differences have been observed comparing different population so that several M. persicae populations were, for example, heterozygous for a translocation between autosomes 1 and 3 and this particular rearrangement has been shown to be involved in resistance to organophosphate and carbamate insecticides.

Interestingly, the analysis of mitotic metaphases of a newly isolated M. persicae clone revealed different chromosome numbers ranging from 12 to 17 within each embryo, in place of the standard karyotype consisting of 12 chromosomes. Highly variable karyotypes resulted in the presence of different chromosome numbers between embryos from different individuals within the same asexual lineage, between single embryos from the same individual and within embryos. Aphid chromosome unusually had recurrent fissions that resulted in a continuous change of both chromosome number and structure.

How can aphids change their karyotype so quickly? Aphids show more variations in the karyotype than other organisms since they have holocentric chromosomes with kinetic activity spread along the whole chromosome axis. Hence, chromosomal fragments can contact the microtubules and move properly in the daughter cells during cell division.

Chromosome instability is a peculiar feature of malignant cells, whereas it is a very rare phenomenon in physiological situations. In this connection, variations in chromosome number are largely utilised for taxonomic and phylogenetic speculations. Among insects, highly variable karyotypes are reported in few cases such as the ants Diacamma ceylonense and Diacamma nilgir, where the presence of intra-tissue, intra-individual and inter-individual variability in the karyotype was assessed in both males and females making aphids an intriguing model for the study of chromosome evolution.

What happen to telomeres? The holokinetic structure of aphid chromosomes that ensure the attachment of spindle microtubules along most of the chromosome length is itself not sufficient to stabilize chromosome fragments, since chromosomal breakpoints may be highly unstable displaying a facility to fuse with other broken ends. The breakpoints need therefore to be stabilized before transmission of chromosomal fragments to the daughter cells through a de novo telomere synthesis, generally involving the addition of repetitive telomeric sequences at the breakpoints by the enzyme telomerase. Indeed, the essential function of telomeres is to protect chromosome ends from nucleolytic degradation, chromosome fusion and the inappropriate engagement of checkpoint signalling, so that the addition of telomere repeats results in the stabilization of the new chromosome ends and allows the resumption of cell cycling. In the absence of healing, unrepairable double-strand breaks generally lead to programmed cell death. Aphid telomerase gene is expressed in all the tissues so that chromosomal fragments can be inherited without any failure in some checkpoint presence.

In view of the presence of mechanisms to stabilize and inherit chromosome fragments without effect on viability are aphid immortal insects? Someone speculated that the reply could be yes!

Reference: Monti,V., Mandrioli, M., Rivi, M., Manicardi, G.C. (2012). The vanishing clone: karyotypic evidence for extensive intraclonal genetic variation in the peach potato aphid, Myzus persicae (Hemiptera: Aphididae) Biological Journal Linnean Society, 105: 350-358.

This post partecipates to the Molbiol Carnival hosted by Scientific American!

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