The potential role of chromosome telomere resetting consequent upon sex in the population dynamics of aphids: an hypothesis

Models of population structure have emphasized the importance of sex in maintaining lineages. This is because, despite the well known ‘two‐fold cost of sex’ compared with asex, it is considered that recombination rids the genome of accumulated mutations and increases its potential for adaptive variation. However, asexual lineages of eukaryotic organisms can also rapidly gain genetic variance directly by various mutational processes, thereby proving that so‐called ‘clones’ do not have strict genetic fidelity ( Lushai & Loxdale, 2002 ; Loxdale & Lushai, 2003a ), whereas the variation so produced may well have adaptive advantage during the evolutionary process. This being so, obligated asexuals or cyclical parthenogens that occasionally indulge in sexual recombination (‘rare sex’) cannot be deemed as ‘evolutionary dead‐ends’( Lushai, Loxdale & Allen, 2003a ). In addition, the persistence of asexual lineages (i.e. lineage longevity) may also involve the integrity of the telomere region, the physical end of the chromosomes ( Loxdale & Lushai, 2003b ). In this earlier study on this topic, we argued that the persistence and ultimate senescence of eukaryotic cell lineages (based upon the frequency of ‘capped’ and ‘uncapped’ chromosomes related to telomere functionality; Blackburn, 2000 ) may directly relate to the survival and persistence of lineages of whole asexual organisms. Aphids are a good model system to test this hypothesis because they show a variety of sexual/asexual reproductive strategies, whereas their mode of asexual reproduction is of the mitotic (= apomictic) type. We also suggested that many aphid lineages require occasional or even rare sexual recombination to re‐set telomere length to allow lineages to persist. Ample empirical evidence from diverse taxa, lineages, and different developmental stages now reveals that the telomere states are indeed re‐set by recombination (homologous or meiotic), thereby rejuvenating the lineage in question. The generational clock element of telomeric functionality has also been successfully described in artificially‐induced mammalian clonal systems. It thus appears that telomere function is a central molecular mechanism instigating and promoting lineage continuity per se. By contrast, we hypothesized that other long‐lived asexuals, or the rare category of ancient asexuals such as bdelloid rotifers, have compensatory mechanisms for maintaining chromosome functional integrity, which are somewhat different from conventional telomeric repeats. In the present study, we carry the analogy between eukaryotic cell functionality and aphid lineages a stage further. Here, we hypothesize that the changing frequency of capped and uncapped telomeres, progressing to senescence in a stochastic manner, may be an underlying factor that significantly contributes to population dynamics in asexual lineage evolution. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 719–728.