Parasites and Sexual Reproduction in Psychid Moths

Abstract

Abstract. Persistence of sexual reproduction among coexisting asexual competitors has been a major paradox in evolutionary biology. The number of empirical studies is still very limited, as few systems with coexisting sexual and strictly asexual lineages have been found. We studied the ecological mechanisms behind the simultaneous coexistence of a sexually and an asexually reproducing closely related species of psychid moth in Central Finland between 1999 and 2001. The two species compete for the same resources and are often infected by the same hymenopteran parasitoids. They are extremely morphologically and behaviorally similar and can be separated only by their reproductive strategy (sexual vs. asexual) or by genetic markers. We compared the life-history traits of these species in two locations where they coexist to test predictions of the cost-of-sex hypothesis. We did not find any difference in female size, number of larvae, or offspring survival between the sexuals and asexuals, indicating that sexuals are subject to cost of sex. We also used genetic markers to check and exclude the possibility of Wolbachia bacteria infection inducing parthenogenesis. None of the samples was infected by Wolbachia and, thus, it is unlikely that these bacteria could affect our results. We sampled 38 locations to study the prevalence of parasitoids and the moths' reproductive strategy. We found a strong positive correlation between prevalence of sexual reproduction and prevalence of parasitoids. In locations where parasitoids are rare asexuals exist in high densities, whereas in locations with a high parasitoid load the sexual species was dominant. Spatial distribution alone does not explain the results. We suggest that the parasite hypothesis for sex may offer an explanation for the persistence of sexual moths in this system. Key words. Bag worm moth, cost of sex, parasite hypothesis, parthenogenesis, Red Queen hypothesis, Wolbachia.Received October 8, 2003. Accepted February 9, 2004 Maintenance of sexual reproduction has been a puzzling question in the theory of evolution since it was first raised by Williams (1975), Maynard Smith (1978), and Bell (1982. Many hypotheses have been presented to explain the maintenance of sex (e.g., Kondrashov 1993;Hurst and Peck 1996;Lively 1996; Jokela et al. 2003), since the asexually reproducing morphs could produce offspring more effectively than the sexuals by avoiding the costs of producing males. This cost of sex should finally lead to replacement of sexuals if the all-else-equal assumption is true (Maynard Smith 1978). In the long term, this should lead to natural populations consisting purely of asexually reproducing females, unless there are some short-term advantages of sexual reproduction (e.g., Lively 1996). Such short-term advantages could arise from the genetic recombination in cross-fertilization, which purges deleterious mutations and increases the amount of genetic variation (Muller 1964;Kondrashov 1988;Rice 2002).The importance of variation in the host genotype was further ...

Genetic diversity in populations of asexual and sexual bag worm moths (Lepidoptera: Psychidae)

“…Instead, adaptation to different microclimates or other specific environmental conditions of these locales could explain the presence of many different genotypes, as suggested by Vrijenhoek's [43] frozen niche variation hypothesis. However, we found no significant differences in morphology, size and life-history characters between two different D. fennicella populations that would reflect ecological specialisation [34]. Although several studies have reported allozymes as not neutral (reviewed in [44,45]), in our study there were no indications that they deviate from neutrality, thus these markers are expected to be subjected more to drift than to selection.…”

“…Life cycle from egg to adult takes from one to two years, but the adults only live 3–6 days [33]. S. rupicolella and D. fennicella are very difficult to separate from each other and the only distinctive characters are their reproductive mode and genetic markers [32,34]. In central Finland, these bag worm moth species occur patchily in wooded habitats.…”

“…Kumpulainen et al . [34] found a strong positive correlation between parasite prevalence and the occurrence of sexual reproduction in Finnish bag worm moth populations for three consecutive years. S. rupicolella (sexual) was more abundant where parasitoids were more common, whereas D. fennicella (asexual) was more common in localities where parasitoids were scarce or absent.…”

On the elusiveness of enemy-free space: spatial, temporal, and host-plant-related variation in parasitoid attack rates on three gallmakers of goldenrods

“…For all three herbivores (and regardless of which Solidago species is Epiblema's ancestral host), we observed parasitoid EFS on the novel host at some sites/years, but the reverse at others; even for year/site contrasts where the host providing EFS did not change, the strength of the effect often did. We emphasize that we are not merely documenting spatial and temporal variation in parasitoid attack on a single herbivore-such variation is expected and has been amply documented (e.g., Feeny et al 1985;Mira and Bernays 2002;Stireman and Singer 2002;Singer and Stireman 2003;Kumpulainen et al 2004;Singer et al 2004).…”

“…For several reasons, the selective effect of enemy-free space may resemble a geographic and/or temporal mosaic (Thompson 1994(Thompson , 1997 rather than a simple parasitoid-escape advantage. After all, attack by parasitoids and predators on a given herbivore is often highly variable in space and time (e.g., Feeny et al 1985;Mira and Bernays 2002;Stireman and Singer 2002;Singer and Stireman 2003;Kumpulainen et al 2004;Singer et al 2004), and if nothing else EFS cannot exist at sites or times where attack is negligible on either host (e.g., Mira and Bernays 2002). Furthermore, parasitoids of herbivores with host races or cryptic species on alternative hosts may themselves have evolved specialist races or species (Stireman et al 2006) with the potential for independently varying population dynamics.…”