Figure 3.12. provides a summary of all four experiments for ease of comparison. Unsurprisingly, the weather plays a large part in the numbers of butterflies observed. This appears to be particularly important in experiment four (Table 3.7.), following a severe rain storm on day 3, the numbers of butterflies flying decreases considerably for the next couple of days before rising again, probably due to emergence of new adilts. However, despite the effect of the weather, results strongly suggest that in Fiji male//.
bolina are territorial whereas in Independent Samoa, the females are territorial, being found consistently in the same areas at the same times on consecutive days. No marked Fijian females were recaptured indicating that fem ale//, bolina behave differently in the different populations.
Chapter 3: Extraordinary sex ratios in Independent Samoa 132 0.8 ■a
§
i-0 .6s
0 CC c o V o 0.4 Q. O 0.2 m Experiment 1 □ Experiment 2 ■ Experiment 3 □ Experiment 4Day 2 Day 3 Day 4 Day 5 Day 6
Figure 3.12. Proportion of adults recaptured during consecutive days in all four site fidelity experiments: Experiments 1 and 2 carried out in the Fiji Islands, using m ale//.
bolina (n=20 and n= 16 respectively); experiments 3 and 4 carried out in Independent Samoa using female H. bolina (n=15 and n=17 respectively).
The male killing Wolbachia at high prevalence seems to have an effect on the behaviour of adult H. bolina. At high prevalence of the male killer, females start to behave in the way that males do in uninfected or low prevalence male killer host systems. We might expect to witness female competition for mates, and although certain ‘altercations’ between different females in the field were recorded, so few males were seen in
Chapter 3: Extraordinary sex ratios in Independent Samoa 1 3 3
3.13. Discussion
The H. 6o/mfl/male killing Wolbachia symbiosis in Independent Samoa provides an example of sex ratio distortion in the extreme. It seems incredible that this situation has persisted for at least 80 years (i.e. at least 300 generations) and in all probability,
considerably longer (Hopkins, 1927). The data presented in this chapter represent the highest prevalence of a male killing bacteria ever recorded in a natural host population. This has huge implications on the host population. It can be postulated that such a situation will result in one of three different outcomes for the host population: extinction, evolution of resistance or population damage.
In his 1967 paper, ‘Extraordinary Sex Ratios’, W. D. Hamilton modelled invasion dynamics of selfish genetic elements (Hamilton, 1967). He suggested that if selfish genetic elements were to reach an exceedingly high level of prevalence, the host
population would be damaged and could eventually be driven to extinction due to lack of one sex. Lyttle’s (1977) laboratory study demonstrated Hamilton’s earlier model in artificial caged host populations. His experiments used Drosophila melanogaster as the host of an artificially introduced selfish genetic element, a meiotically driving Y
chromosome. Host extinction was recorded from a number of replicates as the level of infection increased in the artificial laboratory populations. Such effects have not been reported in natural populations but, for obvious reasons, it is difficult to record extinction in nature.
If extinction does not occur, as it clearly has not in the Independent Samoan77. bolina
populations, then we might expect to see evidence of host resistance to the selfish genetic element, as has been previously reported in natural populations of woodlice infected with feminising Wolbachia (Rigaud & Juchault, 1993). Resistance evolution seems a distinct
Chapter 3: Extraordinary sex ratios in Independent Samoa 1 3 4 possibility for the Independent Samoan populations, given the rarity with which infected females produce sons and the scarcity of uninfected females in the population.
Surprisingly, neither extinction nor resistance evolution are seen in if. bolina in Independent Samoa. That is not to say that the Wolbachia male killer ‘monopoly’ in these populations does not have dramatic ‘knock on’ effects on the host species. The resultant lack of male H. bolina in Independent Samoa increases female virginity and decreases female fertility in the study populations. The net result is a decrease in female reproductive success, even when females are mated, as demonstrated by the crossing experiments: Independent Samoan females mated to males from populations in which the male killing Wolbachia is at a much lower, or nonexistent prevalence, showing ‘normal’ levels of fertility.
Based on the significant differences in sizes of spermatophores between males from Independent Samoa and those from other populations, it is tempting to suggest that Independent Samoan males have evolved the ability to partition their ejaculate, reducing the number of sperm allocated per mating. Even virgin Independent Samoan males produce significantly smaller spermatophores than males from populations with much lower prevalences of the Wolbachia male killer. This apparent difference in ejaculate allocation requires more stringent analysis. Butterflies produce two different types of sperm: eupyrene or fertilising sperm, and apyrene non-fertile sperm (Wedell, 2001). It has been demonstrated in Pieris rapae that the proportion of eupyrene and apyrene sperm allocated per mating vary with the degree of sperm competition in the population (Wedell & Cook, 1999). An investigation of H. bolina males from Independent Samoa, Fiji and American Samoa could be carried out, analysing the average proportion of eupyrene and
Chapter 3: Extraordinary sex ratios in Independent Samoa 1 3 5
bolina males would allocate less sperm per ejaculate than males from the other host populations, although we would expect to see a higher ratio of fertilising (eupyrene) sperm reflecting the lack of sperm competition in the Independent Samoan population.
3.13.1. Why has resistance to the Wolbachia male killer not evolved in the