Evidence for frequency‐dependent selection maintaining polymorphism in the Batesian mimic Papilio polytes in multiple islands in the Ryukyus, Japan

Abstract

Batesian mimicry is a well‐studied adaptation for predation avoidance, in which a mimetic species resembles an unpalatable model species. Batesian mimicry can be under positive selection because of the protection gained against predators, due to resemblance to unpalatable model species. However, in some mimetic species, nonmimetic individuals are present in populations, despite the benefits of mimicry. The mechanism for evolution of such mimetic polymorphism remains an open question. Here, we address the hypothesis that the abundance of mimics is limited by that of the models, leading to mimetic polymorphism. In addition, other forces such as the effects of common ancestry and/or isolation by distance may explain this phenomenon. To investigate this question, we focused on the butterfly, Papilio polytes, that exhibits mimetic polymorphism on multiple islands of the Ryukyus, Japan, and performed field surveys and genetic analysis. We found that the mimic ratio of P. polytes was strongly correlated with the model abundance observed on each of the five islands, suggesting negative frequency‐dependent selection is driving the evolution of polymorphism in P. polytes populations. Molecular phylogenetic analysis indicated that the southern island populations are the major source of genetic diversity, and the middle and northern island populations arose by relatively recent migration. This view was also supported by mismatch distribution and Tajima's D analyses, suggesting a recent population expansion on the middle and northern islands, and stable population persistence on the southern islands. The frequency of the mimetic forms within P. polytes populations is thus explained by variations in the model abundance rather than by population structure. Thus, we propose that predation pressure, rather than neutral forces, have shaped the Batesian mimicry polymorphism in P. polytes observed in the Ryukyus.

Population genetic structure and evolution of Batesian mimicry in Papilio polytes from the Ryukyu Islands, Japan, analyzed by genotyping-by-sequencing

“…Strong correlation of the MRs of P. polytes with mimetic model abundance was found in five islands of the Ryukyu, rather than with geographic or genetic distances, incorporating newly added fieldwork data (Tsurui-Sato et al 2019). In particular, the northern island populations were thought to be relatively recent immigrants having experienced population expansion, while their MRs correlated with the local abundance of model species that was probably caused by rapid evolution through NFDS (Tsurui-Sato et al 2019). These results, however, may have suffered from incomplete lineage sorting or other biases because they are primarily based on a single locus.…”

“…In the Ryukyu Islands, some females mimic unpalatable Pachliopta aristolochiae as a defense against avian predators (Uesugi 2000;Katoh et al 2017), while others resemble males (Figure 1a). Interestingly, the MRs vary among the Ryukyu Island populations, and tend to be high where more of the model P. aristolochiae are present (Uesugi 2000;Tsurui-Sato et al 2019). In particular, after the model species immigrated to Miyako Island (MYK in Figure 1b) and became established, the MR of this island increased rapidly from 1975 to 1989 (Uesugi 2000), implying local adaptation through NFDS (Tsurui-Sato et al 2019).…”

“…In a previous study, we proposed that negative frequency-dependent selection (NFDS) explains the polymorphic Batesian mimicry of the swallowtail butterfly Papilio polytes L. from the Ryukyu Islands in Japan (Tsurui-Sato et al 2019). The NFDS model (Barrett 1976;Turner 1978;Kunte 2009) predicts that the number of mimics in the population depends on the abundance of the model species in the habitat, because the defensive benefit of mimicry increases when the toxic or unpalatable model is more abundant.…”

“…To evaluate this NFDS model for the maintenance of Batesian mimicry polymorphism, P. polytes from the Ryukyu Islands provides a good model system (Tsurui-Sato et al 2019). This species is a common swallowtail butterfly in Southeast Asia and the southern part of East Asia, and exhibits polymorphic Batesian mimicry in females (Clarke & Sheppard 1972;Ford 1975;Kunte et al 2014;Katoh et al 2017).…”

“…Our previous study (Tsurui-Sato et al 2019) examined the possible association between the MR of P. polytes and the abundance of the mimetic model in the Ryukyu Islands, with respect to the NFDS hypothesis. The alternative, isolation-by-distance view of the MR variation among islands was tested by genetic analyses based on mitochondrial DNA (mtDNA).…”