Fifty-year trend towards suppression of Wolbachia-induced male-killing by its butterfly host, Hypolimnas bolina

Abstract

Some intracellular symbionts of arthropods induce a variety of reproductive alterations in their hosts, and the alterations tend to spread easily within the host populations. A few cases involving the spread of alteration-inducing Wolbachia bacteria in natural populations with time have been reported, but the investigations on the increasing trend in counteracting the bacterial effect on hosts in natural populations (i.e., increased resistance in hosts against the alterations) have been limited. In the present study, the prevalence of an alteration, killing of male Hypolimnas bolina (L.) (Lepidoptera: Nymphalidae) butterflies by their inherited Wolbachia strain in the wild in Japan, was surveyed over a continuous 50-year period, which is far longer than ever before analyzed in studies of dynamics between reproductive alteration-inducing symbionts and their host arthropods. Thus, the results in this study provide the first instance of a long-term trend involving a change in reproductive alteration; and it strongly suggests a change in the opposite direction (i.e., suppression of male-killing) in natural populations. This change in the current combination of the Wolbachia and butterflies appears to be dependent upon the host taxon (race).

Figure 1.

Map of the area (Japan) covered in the present study. The Sakishima Islands, Okinawa Pref., one of the major study areas, are shown in detail in the lower panel. High quality figures are available online.

Figure 2.

Phylogenetic tree of Wolbachia strains originated from various insect species. The tree was generated using the neighbor-joining method based on the numbers of nucleotide differences among taxa. Wolbachi strains are represented by the names of their hosts. Supergroup A strains of Drosophila melanogaster and Hypolimnas bolina are shown as outgroups. Concatenated five gene sequences for MLST were used for the analysis. Bootstrap confidence levels higher than 50% calculated based on 1,000 replications are shown near the branches. STs are sequence types in the MLST system. ST-176 was newly found in the present study. High quality figures are available online.

Figure 3.

Proportion of males in the total number of wild adult Hypolimnas bolina observed in Japan in each 4-year period over the past approximately 50 years from 1959 through 2006. (A) The status of the proportion of males in the major distribution area of Japan, i.e. Okinawa and Kagoshima Prefectures, and the whole of Japan was analyzed. (B) Status of the proportion of males in each race was analyzed. The proportions of males in (A) and (B) were calculated based on the number of H. bolina adults shown in Tables 3A and 3B, respectively. The proportion of males was not calculated if total number of individuals per 4-year period was less than 8. High quality figures are available online.