Persistence of an extreme sex-ratio bias in a natural population

Abstract

The sex ratio is a key parameter in the evolution and ecology of a species. Selfish genetic elements that bias the sex ratio of affected individuals are well known and characterized, but their effect on populations has been considered limited, because either the element does not achieve high prevalence or the host rapidly evolves resistance to the distorting element, reducing its prevalence. We tested whether the host necessarily prevails by using a butterfly system where records from the early part of the 20th century reported extreme sex-ratio bias in nature. We reexamined this population and found the bias was present today, 400 generations after the original record, with a population sex ratio of 100 females per male. The sex-ratio bias was associated with the presence of a heritable male-killing Wolbachia infection in 99% of adult females, against which the host butterfly has failed to evolve resistance. The resultant dearth of males causes an average 57% reduction in the reproductive output of adult females. Persistence of the population despite the very high frequency of the sex-ratio distorter appears to be associated with the ability of males to mate >50 times in their life combined with a high intrinsic rate of increase of the species.

Distribution and Evolutionary Impact of Wolbachia on Butterfly Hosts

“…To answer this question, they compare their results with other island with lower Wolbachia infection in H. bolina. They interpret that low male frequency leads to 57 % loss of reproductive output [41]. They further found that male spermatophores of H. bolina from Independent Samoa were almost half the diameter of spermatophores produce by H. bolina from neighboring island.…”

“…In 2004, Dyson and Hurst [41] had shown that this extreme sex bias is persistent at least 400 generation after its first record in Independent (Western) Samoa. They further concluded that, sex bias is because of high prevalence of MK Wolbachia and not because of parthenogenesis.…”

The dynamic relationship between polyandry and selfish genetic elements

“…uninfected females and infected males), but solely linked to the magnitude of the fertility reduction of male carriers. In Hypolimnas bolina butterflies for example, many South Pacific populations harbour a male-killing strain of Wolbachia [65]. Intriguingly, different populations have different frequency of male killers that is associated with differences in degree of female-biased sex ratio, with a higher frequency of male killers associated with a more severely female-biased population sex ratio [66].…”

Incomplete offspring sex bias in Australian populations of the butterfly Eurema hecabe

“…Lepidoptera have proven an excellent group for exploring arthropodendosymbiont dynamics (Dyson and Hurst, 2004;Hornett et al, 2006;Sugimoto and Ishikawa, 2012). This group harbors bacterial symbionts such as Spiroplasma and Wolbachia collectively known to impose CI, male killing and feminization (Jiggins et al, 2000;Hiroki et al, 2004;Charlat et al, 2005).…”

“…This group harbors bacterial symbionts such as Spiroplasma and Wolbachia collectively known to impose CI, male killing and feminization (Jiggins et al, 2000;Hiroki et al, 2004;Charlat et al, 2005). Studies of butterfly male-killing have yielded valuable insights into host-symbiont coadaptation, including the genetic and biogeographic basis of nuclear host suppression (Dyson and Hurst, 2004;Hornett et al, 2006Hornett et al, , 2008Charlat et al, 2007b, c). Lepidopterans have also informed the study of feminization, primarily via the work in Wolbachia-infected Ostrinia moths (Crambidae) and Eurema butterflies (Pieridae).…”