Research Article Essay

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A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly
Hideki Nishikawa1,11, Takuro Iijima1,11, Rei Kajitani2, Junichi Yamaguchi1, Toshiya Ando1,3, Yutaka Suzuki4, Sumio Sugano5, Asao Fujiyama6,7, Shunichi Kosugi8, Hideki Hirakawa8, Satoshi Tabata8, Katsuhisa Ozaki9, Hiroya Morimoto2, Kunio Ihara10, Madoka Obara10, Hiroshi Hori10, Takehiko Itoh2 & Haruhiko Fujiwara1

In Batesian mimicry, animals avoid predation by resembling distasteful models. In the swallowtail butterfly Papilio polytes, only mimetic-form females resemble the unpalatable butterfly Pachliopta aristolochiae. A recent report showed that a single gene, doublesex (dsx), controls this mimicry1; however, the detailed molecular mechanisms remain unclear. Here we determined two whole-genome sequences of P. polytes and a related species, Papilio xuthus, identifying a single ~130-kb autosomal inversion, including dsx, between mimetic (H-type) and non-mimetic (h-type) chromosomes in P. polytes.
This inversion is associated with the mimicry-related locus H, as identified by linkage mapping. Knockdown experiments demonstrated that female-specific dsx isoforms expressed from the inverted H allele (dsx(H)) induce mimetic coloration patterns and simultaneously repress non-mimetic patterns.
In contrast, dsx(h) does not alter mimetic patterns. We propose that dsx(H) switches the coloration of predetermined wing patterns and that female-limited polymorphism is tightly maintained by chromosomal inversion.

P. polytes is known to exhibit female-limited Batesian mimicry. The females have two forms: a non-mimetic form (cyrus), with wing pat- terns identical to those of monomorphic males, and a mimetic form (polytes) resembling the toxic model P. aristolochiae (Fig. 1a). This polymorphism is controlled by a single autosomal locus H, and the mimetic phenotype (genotype HH or Hh) is dominant2. There are two models of the underlying gene encoded in the H locus: a conceptual ‘supergene’ consisting of a series of neighboring genes tightly linked to one another3, or a regulatory gene controlling unlinked downstream genes that affect the color pattern4. It has been demonstrated that a supergene is created and fixed by chromosomal rearrangements in Heliconius numata, a species exhibiting Müllerian mimicry5. In addition, a recent study on P. polytes has shown that the mimetic phenotype is controlled by dsx, which was suggested to be fixed by chromosomal inversion1. However, the chromosomal structure and detailed molecular mechanisms involved in the female-limited poly- morphic mimicry in P. polytes remain obscure.
Kunte et al. identified the H locus as corresponding to dsx1; in this study, we performed further crosses that confirmed this result using non-mimetic individuals of P. polytes and mimetic individuals of the subspecies P. p. alphenor (also known as Papilio alphenor). Using DNA fragment-length polymorphisms, we mapped the H locus in P. polytes to a region spanning 800 kb on chromosome 25 (Fig. 1b,c). In addition, analysis of SNPs in the 800-kb region using 54 P. polytes females cap- tured on the Ryukyu Islands, Japan, showed that 8 SNPs in dsx were associated with the mimetic phenotype (P < 1 × 10−10; Fig. 1d).
Following this analysis, we determined the whole-genome sequences of P. polytes (Hh mimetic female) and the related species
P. xuthus for comparison using the HiSeq 2000 and HiSeq 2500 sys- tems (Supplementary Table 1). The quality of the assembled scaffolds for both species was high enough for these to be used as reference genomes (scaffold N50 values: P. polytes, 3.7 Mb; P. xuthus, 6.2 Mb; Supplementary Table 2). The total genome sizes for P. polytes and
P. xuthus were 227 Mb and 244 Mb (Supplementary Table 2), encod- ing 12,244 and 13,102 predicted protein-coding genes, respectively (Supplementary Table 3). The number of ortholog groups among 5 Lepidoptera species is shown in Figure 2a, and a phylogenetic tree of 2,077 of
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