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Reproductive Biology of Female Swallowtail Butterflies Pertaining to the Pre- and Post- Copulatory Mate Choice

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Reproductive Biology of Female Swallowtail Butterflies Pertaining to the Pre- and Post- Copulatory Mate Choice Reproductive Biology of Female Swallowtail Butterflies Pertaining to the Pre- and Post- Copulatory Mate Choice 著者 佐々木 那由太 内容記述 この博士論文は内容の要約のみの公開（または一部 非公開）になっています year 2016 その他のタイトル 交尾前と交尾後の配偶者選択に関連したアゲハチョ ウ類の雌の繁殖生物学 学位授与大学 筑波大学 (University of Tsukuba) 学位授与年度 2015 報告番号 12102甲第7754号 URL http://hdl.handle.net/2241/00144280 Reproductive Biology of Female Swallowtail Butterflies Pertaining to the Pre- and Post- Copulatory Mate Choice A Dissertation Submitted to the Graduate School of Life and Environmental Sciences, the University of Tsukuba in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Doctor of Philosophy in Science （Doctoral Program in Integrative Environmental Sciences ） Nayuta SASAKI C O N T E N T S ABSRACT 1 GENERAL INTRODUCTION 2 Pattern of sperm storage and migration in the reproductive tract CHAPTER 1 of the swallowtail butterfly Papilio xuthus : cryptic female choice 8 after second mating Effect of sperm ejection by females on male fertilization success in CHAPTER 2 the swallowtail butterfly, Papilio xuthus L. (Lepidoptera: 28 Papilionidae) Indicators of recent mating success in the pipevine swallowtail CHAPTER 3 butterfly ( Battus philenor ) and their relationship to male 49 phenotype GENERAL DISCUSSION 81 ACKNOWLEDGEMENTS 89 i T A B L E L I S T CHAPTER 2 Table 1. Body mass of both sexes and the ejaculate mass for each mating group 43 (mean±SD). Table 2. Number of eggs laid (mean±SD) and hatching rate (mean±SE) for each 44 mating group. Table 3. Results of the generalized linear model of factors that contribute to 45 variation in P 2 values. CHAPTER 3 Table 1. A summary of the state of reproductive tract components of 68 males 71 caught in the field. A plus sign means that the state of that component met the criteria we set for indicating the male recently mated. A minus sign means it did not meet the criteria. In later analysis, any group that met two or more of the criteria (Groups E to H), and males that met none of the criteria (Group A) were used as recently mated males and as not recently mated males, respectively. Table 2. Spearman correlation coefficients for the relationship between male age 72 and the various color parameters for the dorsal hindwing coloration. Significant correlation between intensity and chroma, chroma and hue, and chroma and age-class were found. Table 3. Results of an ANOVA (GLM) of factors that contribute to variation in 73 recent mating success of wild males. Effect of hue and age-class on male recent mating success were significant. ii F I G U R E L I S T CHAPTER 1 Fig. 1. A schematic representation of the bursa copulatrix, including a 24 spermatophore and accessory substances, and the spermatheca in a single mated female (after Watanabe et al. 2000). Fig. 2. Changes in the percentage of the females with spermathecae 25 containing sperm after the first mating. Numerals indicate the number of females dissected. Fig. 3. Changes in the percentage of the females in relation to sperm 26 occupied in the spermatheca after the second mating. Numerals indicate the number of females dissected. Fig. 4. Spermatophore mass of the second male in relation to the quantity 27 and quality of sperm in the spermatheca of the remated females 8 h after the termination of the copulation (+SE). The different letter indicates a significantly difference at the probability less than 0.05, using Dunnett T3-test. Numerals indicate the number of females examined. CHAPTER 2 Fig. 1. A schematic representation of the Papilio xuthus bursa copulatrix, 46 including a spermatophore and accessory gland substances, and the spermatheca in a single mated female (after Watanabe et al. (2000)). Fig. 2. The frequency distribution of P 2 values in 23 twice-mated Papilio 47 xuthus females. Fig. 3. Relationship between the relative ejaculate mass (log(weight gain of 48 females due to the second mating/that of the first mating)) and P 2 values in 23 twice-mated Papilio xuthus females. Statistical results are shown in Table 3. CHAPTER 3 Fig. 1. A schematic representation of the internal reproductive organs of a B. 74 philenor male. Fig. 2. Photographs of representative simplexes of a virgin male (A) and a 75 male just after the termination of copulation (B) in B. philenor. Each simplex leads to the aedeagus and the duplex at left-hand and right-hand end of the photograph, respectively. iii Fig. 3. Simplex mass (A), length (B), and transparency difference (C) in 76 virgin males as a function of time since eclosion (mean±S.D.). The number in each bar represents sample size. ANOVA revealed no significant effect of age of virgin males on mass (F2,21 =1.554, p=0.237), length ( F2,21 =2.276, p=0.130) and transparency difference (F2,21 =0.475, p=0.629) of simplex. Fig. 4. Simplex mass (A), length (B), and transparency difference (C) of 77 mated males as a function of the male’s age at the time of copulation (mean±S.D.). The number in each bar represents sample size. ANOVA revealed no significant effect of males’ age at mating on mass ( F2,16 =0.027, p=0.974), length ( F2,16 =1.331, p=0.296) and transparency difference ( F2,16 =0.170, p=0.845) of simplex. Fig. 5. Simplex mass (A), length (B), and transparency difference (C) of 78 simplex for virgin males (V, zero, three, six days old) and for mated males (one, three, five days old) dissected at various number of days after mating (mean±S.D.). The number in each bar represents sample size. ANOVA revealed significant effect of days since the mating on mass ( F5,61 =59.202, p<0.001), length ( F5,55 =42.770, p<0.001) and transparency difference ( F5,55 =17.139, p<0.001) of simplex. *,** and *** represent p<0.05, p<0.01 and p<0.001 in Tukey’s HSD test, respectively. Fig. 6. The hue (wavelength of maximum reflectance) of the dorsal hindwing 79 for field-caught males that met the criteria for evidence of having recently mated and those males that did not meet the criteria (±S.E.). Recently mated males had a significantly higher hue value (were greener) than males that had not recently mated. Statistical results are shown in Table 3. Fig. 7. Change with age-class in the number of clearly recently-mated males 80 (light-gray bar), clearly not-recently-mated males (black bar) and males of uncertain recent mating history (dark-gray bar) for field-caught males. Older males were more likely to mate than younger males. Statistical results are shown in Table 3. General Discussion Fig. 1. The P2 value of females to which larger spermatophores had been 88 transferred from the first than from the second male, and those females to which larger spermatophores had been transferred from the second than the first male (±S.E.). iv ABSTRACT One of the important ways for a female to obtain high reproductive success is to increase the survivability and/or reproduction of her offspring. Then, the quality of sperm used for fertilizing eggs must be critical for female perspective. In swallowtail butterflies, because females have a specially adapted sperm storage organ for fertilization, spermatheca, and because female multiple mating is common, sperm from different males could have a chance to coexist within a female. To increase the reproductive success, multiple mated females should choose sperm derived from different males for fertilization. This is a so-called cryptic female choice. To clarify the mechanisms of cryptic female choice in a polyandrous swallowtail butterfly, Papilio xuthus , sperm storage process and the paternity of twice-mated females were examined. Re-mated females ejected first male’s sperm from the spermatheca when the second male transferred a lager spermatophore than that of first male, resulting in the biased paternity for the male that had transferred a larger spermatophore. In addition, the significant effect of male dorsal hindwing coloration on their mating success was demonstrated in a wild population of monandrous swallowtail butterfly, Battus philenor , in which the color of male dorsal hindwing significantly predicted the spermatophore mass. Since male wing color does not affect competitiveness among males, correlation between male wing color and mating success must be caused by the female choice. Therefore, females in both polyandrous and monandrous species might exercise choice for obtaining sperm of males that can produce a large spermatophore, though the timing of female choice was different between species. Keywords : cryptic female choice; P 2 value; pre-copulatory mate choice; simplex; spermatophore; sperm ejection; swallowtail butterflies; wing coloration - 1 - GENERAL INTRODUCTION Sexual selection is an evolutionary process that arises from individual variation of fitness, mainly due to the reproductive success rather than its survival (Andersson 1994). A traditional example is the evolution of the long tail in the male guppy, which seemed to be a disadvantage in survival because of the unskillful for swimming to escape from their predators. However, since females prefer to mate with males with longer and more brilliant tail, males with such a long tail must take high mating success resulting in production of many offspring (Bischoff et al. 1985). Recently, it has been widely accepted that the sexual selection plays an important role in shaping traits including secondary sexual traits, sexual dimorphism, reproductive behavior and so on (e.g. Simmons 2001). Males and females have different behavioral role in sexual selection, due to the limiting factor of reproductive success in respective sex. Bateman (1948) reported a strong relationship between mating and the reproductive success in male fruit flies comparing with females, because of the difference in energetic investment of each sex for their gametes.
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