非洲白鳳蝶的多態型，左上方框內是雄性，線的上方是各種斑蝶與細蝶，線的下方是各型雌性白鳳蝶 photo from mimeticbutterflies.org

標題：Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)


摘要

Several species of swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and nonmimetic. The evolution of such sex-limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a nonmimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species: Papilio phorcas, a nonmimetic species with two female forms, and Papilio dardanus, a female-limited polymorphic mimetic species. Their close relationship indicates that female-limited polymorphism could be a shared derived character of the two species. Here, we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes, showing that they are not sister species and thus that the sexually dimorphic state has arisen independently in the two species. Nonhomology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P. dardanus. McDonald-Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P. dardanus, but not in monomorphic populations, nor in the nonmimetic P. phorcas. Hence, the wing polymorphism does not balance polymorphisms in engrailed in P. phorcas. Equally, unlike in P. dardanus, none of the SNPs in P. phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, nonmimetic states. While sexual selection may drive male-female dimorphism in nonmimetic species, in mimetic Papilios, natural selection for protection from predators in females is an alternative route to sexual dimorphism.

福翠鳳蝶 (Papilio phocas) 雄性 (上)與雌性 (下)， 另有一型與雄性相似

鳳蝶的雌性多態性與限性擬態的演化起源已經吸引科學家討論好久，但始終還沒找到一個定論。究竟那是個數個物種的共有衍徵？抑或是個別物種的獨有衍徵呢？或許可以從非洲白鳳蝶 (Papilio dardanus) 的例子中看出端倪。

福翠鳳蝶 (Papilio phocas)與非洲白鳳蝶同屬白鳳蝶種群 (dardanus species-group)，有些觀點認為這兩種可能是最近緣的種類。福翠鳳蝶同樣是只有雌性多態型，但不同的是其不參與擬態。也就是說，如果系統發生學的分析支持這兩個物種是姊妹群，那麼就支持雌性多態性的單一起源。

這個研究以基因體層級大規模的分析，以3964個基因與全粒腺體序列推測這兩者間的親緣關係。結果顯示兩者並未如預期的是最近的姊妹群。另外，此團隊也對控制擬態斑紋的engrailed基因的單核苷酸多態性 (SNP, Single Nucleotide Polymorphism)做分析，在白鳳蝶的多態型族群中偵測到平衡選擇 (balancing selection)的特徵，而在單態型與福翠鳳蝶的族群中都沒有。在非擬態的福翠鳳蝶的SNP分析中，engrailed基因也與雌性多態無關。根據以上資料可以推論，這兩個物種的雌性多態性是起源於單態且非擬態的狀態獨立演化而來，進而形成性雙型性。非擬態的物種的性雙型性可能是由性擇推動，而擬態物種的性雙型性來自天擇作用於雌性，讓這兩個看似相似的現象有著截然不同的機制。

photo from Papilio dardanus (wiki)

標題：Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection.

摘要

The history of 20th Century evolutionary biology can be followed through the study of mimetic butterflies. From the initial findings of discontinuous polymorphism through the debates regarding the evolution of mimicry and the step-size of evolutionary change, to the studies on supergene evolution and molecular characterisation of butterfly genomes, mimetic butterflies have been at the heart of evolutionary thought for over 100 years. During this time, few species have received as much attention and in-depth study as Papilio dardanus. To assist all aspects of mimicry research, we present a complete data-derived overview of the extent of polymorphism within this species. Using historical samples permanently held by the NHM London, we document the extent of phenotypic variation and characterise the diversity present in each of the subspecies and how it varies across Africa. We also demonstrate an association between ‘‘imperfect’’ mimetic forms and the transitional race formed in the area where Eastern and Western African populations meet around Lake Victoria. We present a novel portal for access to this collection, www.mimeticbutterflies.org, allowing remote access to this unique repository. It is hoped that this online resource can act as a nucleus for the sharing and dissemination of other collections databases and imagery connected with mimetic butterflies.

非洲白鳳蝶的多態型，左上方框內是雄性，線的上方是各種斑蝶與細蝶，線的下方是各型雌性白鳳蝶 photo from mimeticbutterflies.org

非洲的白鳳蝶(Papilio dardanus)是知名的貝氏擬態的鳳蝶，其豐富的多態型各自擬態非洲各地的細蝶、斑蝶等不好吃的種類。白鳳蝶的擬態實際上只有雌性參與其中，而雄性只有一種型態，在多態型的雌性中，除了擬態各種不同的蝴蝶外，神奇的也存在雄性型的雌性。

1960年代，透過孟德爾式的遺傳學雜交試驗瞭解不同族群間的斑紋變化，而且結果顯示白鳳蝶的斑紋變化是來自一個超基因；到了2008年，基於現代的分生技術，終於找到超基因的位置。即使如此，雌性的型態實在太多了，除了上面這些看起來精準擬態的斑紋外，也有更多看起來是中間型的種類，因此雖然已經研究到基因體層級的情況下，基礎的斑紋與地理分佈還沒有整體性的調查過。

雌性各種不同的型與名稱 photo from Fig. 1

這篇透過英國倫敦自然史博物館(the Natural History Museum, London)的極大量鱗翅目館藏，蒐集標籤上的採集資訊，將採集的地點轉換成現代的地點並查出座標，把各個不同的斑紋分類後，再轉換為二維座標系統輸入地理資訊系統 (GIS)，把各個不同的斑紋分類後，就能每個型態的分佈呈現在現代的地圖上，並且透過採集點的連線，推估分佈範圍。

取樣密度與地點 photo from Fig. 3 各型的分佈範圍 photo from Fig. 6

結果就如上圖，把大部分的斑紋的分佈範圍推估出來，而那些看起來不完美擬態的斑紋分佈於維多利亞湖附近，支持這是西部與東部族群相遇的雜交區。

中間型的分佈區域 photo from Fig. 7

這分析的概念很簡單，但卻是瞭解一個擬態群的多樣性最快的方式，而且最重要的，這仰賴保存完整與大量的標本館藏。這樣的研究說明透過良好的想法與完整的分析，即使基礎的研究也能從中得到大量的資訊，也更凸顯標本蒐藏的重要性。

photo from K. Kunte

標題：A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly.

摘要

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 mimicry; 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.

photo from Fig 3

基因knockdown後，不同處理的斑紋表現 photo from Fig. 5

標題：A test of fundamental questions in mimicry theory using long-term datasets

摘要

Since the phenomenon of mimicry was first described by Bates in 1862 it has become one of the foundational examples of adaptive evolution. Numerous subcategories of mimicry and dozens of hypotheses pertaining to its evolution and maintenance have been proposed. Many of these hypotheses, however, are difficult to test in experimental settings, and data from natural observations are often inadequate. Here we use data from a long-term survey of butterfly presence and abundance to test several hypotheses pertaining to Batesian and female-limited polymorphic mimicry (FPM; a special case of Batesian mimicry). We found strong evidence that models outnumber mimics in both mimicry systems, but no evidence for an increase in relative abundance of FPM mimics to their Batesian counterparts. Tests of the early-emergence/model first hypothesis showed strong evidence that the Batesian mimic routinely emerges after the model, while emergence timing in the FPM system was site specific, suggesting that other ecological factors are at play. These results demonstrate the importance of long-term field observations for testing evolutionary and ecological hypotheses.
如果擬態群在自然的情況下是有效的，那麼這個擬態群可能符合一些基本的前提，像是model比起mimic來說數量較多、比較難吃、時序上比較早出現等等，都是這個擬態群「應該」要符合的。雖說如此，能夠支持這些基本假設的證據卻是少之又少，也就代表這些基本的假設究竟是科學家自己的想像，還是真正發生在自然界呢？

這個研究透過累積十年的蝴蝶記錄資料來探討這個問題，資料記錄的地點在北美洲，分別是Gates Canyon、Washington與Lang Crossing（詳細資訊見butterfly.ucdavis.edu），記錄的時間大約是每14天一次，累積了1999-2010間的資料。

他們想要討論的問題在於如果貝氏擬態的mimic太多，會導致整個系統的保護作用降低或失效，因此mimic絕對不能比model還多，因此一個可能性就是「model在自然界中絕對數量比mimic多」，另一個可能性是如果mimic只有其中一個性別擬態，那麼相對來說mimic的數量也會減少，因此他們選了兩個系統，其中一個是代表貝氏擬態的系統，Adelpha californica (model)與Limenitis lorquinii (mimic)（見上圖），另一個是雌性擬態的系統（見下圖）。

結果顯示兩個系統中，model的數量都遠多於mimic。發生的時序上來說，貝氏擬態的mimic出現時序都晚於其model，而雌性擬態的物種出現則局現在某幾個地方，可能有其他的生態因子限制其分佈。

標題：Prey from the eyes of predators: Color discriminability of aposematic and mimetic butterflies from an avian visual perspectives

摘要

Predation exerts strong selection on mimetic butterfly wing color patterns, which also serve other functions such as sexual selection. Therefore, specific selection pressures may affect the sexes and signal components differentially.We tested three predictions about the evolution of mimetic resemblance by comparing wing coloration of aposematic butterflies and their Batesian mimics: (a) females gain greater mimetic advantage than males and therefore are better mimics, (b) due to intersexual genetic correlations, sexually monomorphic mimics are better mimics than female-limited mimics, and (c) mimetic resemblance is better on the dorsal wing surface that is visible to predators in flight. Using a physiological model of avian color vision, we quantified mimetic resemblance from predators’ perspective, which showed that female butterflies were better mimics than males. Mimetic resemblance in female- limited mimics was comparable to that in sexually monomorphic mimics, suggesting that intersexual genetic correlations did not constrain adaptive response to selection for female-limited mimicry. Mimetic resemblance on the ventral wing surface was better than that on the dorsal wing surface, implying stronger natural and sexual selection on ventral and dorsal surfaces, respectively. These results suggest that mimetic resemblance in butterfly mimicry rings has evolved under various selective pressures acting in a sex- and wing surface-specific manner.

這篇的中心思想就想要測試三個假設 1) 雌性擬態的精確度比雄性好 2) 單型性擬態的比雌性擬態的物種精確 3) 擬態斑紋在背面的比在腹面的精確。作者想要知道這些現象是不是普遍存在於擬態的蝴蝶中，於是想說「如果從鳥類的視覺來看的話，會不會有差異呢？。」，就用了測量標本的反射光譜，得到某些數據，然後套入鳥類的視覺模型來看看這些擬態的蝴蝶會不會有差異。整個概念就是當把得到的數據套入模型後，比較model與mimic得到的結果，然後統計有沒有顯著差異。結果顯示雌性的擬態比雄性精確，雌性擬態與單型性的物種相比無差異，在背側斑紋比在腹側斑紋精確。

這個結果的確顯示了某些選汰壓力的作用方向，但這個文章中應該只是要展現這有某種演化趨勢，可是缺少考量某些多態型的物種（如大鳳蝶），或是不同的物種在自然界中行為的差異，或許會導向不同的結果與解釋。