Large Population Size Predicts the Distribution of Asexuality in Scale Insects

Abstract

Understanding why some organisms reproduce by sexual reproduction while others can reproduce asexually remains an important unsolved problem in evolutionary biology. Simple demography suggests that asexuals should outcompete sexually reproducing organisms, because of their higher intrinsic rate of increase. However, the majority of multicellular organisms have sexual reproduction. The widely accepted explanation for this apparent contradiction is that asexual lineages have a higher extinction rate.A number of models have indicated that population size might play a crucial role in the evolution of asexuality. The strength of processes that lead to extinction of asexual species is reduced when population sizes get very large, so that the long-term advantage of sexual over asexual reproduction may become negligible. Here, we use a comparative approach using scale insects (Coccoidea, Hemiptera) to show that asexuality is indeed more common in species with larger population density and geographic distribution and we also show that asexual species tend to be more polyphagous. We discuss the implication of our findings for previously observed patterns of asexuality in agricultural pests. K E Y W O R D S :General purpose genotype, parthenogenesis, polyphagy, population size, scale insects.

What does the geography of parthenogenesis teach us about sex?

“…Expanding the discussion to other groups is crucial to determine if asexuality affects distribution patterns universally and in a consistent fashion (a best-case scenario, because then geographic parthenogenesis could give the crucial clue to the mystery of the persistence of sex as a whole), or if recurring geographic patterns are merely a quirky phenomenon restrained to a few groups. In the latter case, it could heavily interact with ecological specificities of these groups to explain the distribution of their asexual forms (as already pointed out in [10,19,130]). For instance, Asteraceae are widespread exploiters of pioneer habitats [142].…”

“…Ross et al [130] found that in scale insects, asexuality is more common in polyphagous, pest or widespread species, and turn the traditional causal argument around: instead of explaining their distribution by their reproductive mode, they propose that species that produce very large populations in the first place resist Muller's ratchet for longer, thus remaining observable today. In support of this direction of causation, they also report that sexual species of genera containing parthenogens have relatively large geographic ranges.…”

“…Successful and widespread species of asexual pathogens exist [144], but to the best of our knowledge, they have not been compared with sexual sister taxa in any geographic context. Being an agricultural pest has also been shown often to be associated with parthenogenesis [12,130]. Some globally spreading pest species of fungi are known to use only vegetative reproduction outside their native range, where they are normally only facultative asexuals, despite several independent introductions being documented [43].…”

The sperm of Matsucoccus feytaudi (Insecta, Coccoidea): Can the microtubular bundle be considered as a true flagellum?

“…This type of reproduction has not yet been reported so far (Riom and Fabre, 1979), even though it is well known among Homoptera (Nur, 1971). A facultative parthenogenesis can occur when population size gets very large, as it has been reported by Ross et al (2013): the finding might explain why it has never been reported so far. The absence of synaptonemal complexes supports our result which could also have applicative consequences: to date, in fact, the biological control of M. feytaudi has been carried out by a sex-pheromone-based mass trapping, which aims to eliminate only the males (Sciarretta, personal communication).…”

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“…4, S6). A similar pattern was suggested to occur in (diploid) parthenogenetic scale insects (Ross et al 2013), and emphasizes that large population sizes of sexuals are paramount in the origin and/or evolutionary success of derived parthenogenetic lineages. Large population sizes should favor the evolution of parthenogenesis because more mutants capable of parthenogenesis are expected in species with larger population size.…”