Adelpha iphiclus photo from learnaboutbutterflies.com

Adelpha serpa photo from learnaboutbutterflies.com

標題：Complex dynamics underlie the evolution of imperfect wing pattern convergence in butterflies


摘要

Adaptive radiation is characterized by rapid diversification that is strongly associated with ecological specialization. However, understanding the evolutionary mechanisms fueling adaptive diversification requires a detailed knowledge of how natural selection acts at multiple life-history stages. Butterflies within the genus Adelpha represent one of the largest and most diverse butterfly lineages in the Neotropics. Although Adelpha species feed on an extraordinary diversity of larval hosts, convergent evolution is widespread in this group, suggesting that selection for mimicry may contribute to adaptive divergence among species. To investigate this hypothesis, we conducted predation studies in Costa Rica using artificial butterfly facsimiles. Specifically, we predicted that nontoxic, palatable Adelpha species that do not feed on host plants in the family Rubiaceae would benefit from sharing a locally convergent wing pattern with the presumably toxic Rubiaceae-feeding species via reduced predation. Contrary to expectations, we found that the presumed mimic was attacked significantly more than its locally convergent model at a frequency paralleling attack rates on both novel and palatable prey. Although these data reveal the first evidence for protection from avian predators by the supposed toxic, Rubiaceae-feeding Adelpha species, we conclude that imprecise mimetic patterns have high costs for Batesian mimics in the tropics.

悌蛺蝶屬 (Adelpha) 主要分佈於新熱帶區，是個物種多樣性極高的複雜類群，目前包含大約85個已知種。這麼高多樣性的類群當然吸引科學家的目光，除了高多樣性的快速演化與起源在近年的相關研究，另一個關注的焦點在其中有一個翅紋樣式在整個屬內多次演化出現，雖然一直被認為是屬內的擬態關係，但相關研究其實不多。

悌蛺蝶屬 (Adelpha)的翅紋多樣性與分布 photo from Lynsey Bunnefeld

photo from Finkbeiner et al. 2012

這個研究在哥斯大黎加進行，在野外針對應該是被擬態者，專食於茜草科的 Adelpha iphiclus ，與另一種廣食種 Adelpha serpa，測試兩者間的翅紋是否存在擬態關係，亦或是單純的趨同。為何是茜草科呢？數個研究指出茜草科的物種含有會讓草食動物避忌的植物鹼化合物，因此專食於茜草科的物種也很有可能在體內存有這類化合物，讓天敵避開 A. iphiclus。實驗用的蝴蝶是將紙翅膀印出後，黏在黏土做的身體上 (如右圖)，並且以光學的方法確定其反射光譜與真實的蝴蝶相似後，再放至野外進行實驗，也就是如果在環境中的捕食者已經被「教育」過了，那麼應該會避免 A. iphiclus，而如果與 A. serpa 間有擬態關係的話，那麼兩者間的被攻擊率應該會十分接近。

本實驗中所使用的物種與統計結果

這個研究挑戰了所謂傳統的擬態群，而也發現令人驚訝的結果，這說明長久以來認定的擬態群可能只侷限在人類的觀點中。作者也並沒有把話說死，直到最後仍用「貝氏的不精確擬態」來描述這兩者間的關係。這個研究的結果也應該提醒了相關研究者，擬態現象的檢測，仍要考慮捕食者視覺，各種生態因子的交互作用，其中的機制可能並非放諸四海皆準。


相關文獻

• Mullen SP, Savage WK, Wahlberg N & Willmott KR. 2011. Rapid diversification and not clade age explains high diversity in neotropical Adelpha butterflies. Proceedings of the Royal Society B: Biological Sciences 278: 1777–1785
• Ebel ER, Dacosta JM, Sorenson MD, Hill RI, Briscoe AD, Willmott KR & Mullen SP. 2015. Rapid diversification associated with ecological specialization in Neotropical Adelpha butterflies. Molecular Ecology 24: 2392–2405

photo from Morpho menelaus (wiki)

標題：Both Palatable and Unpalatable Butterflies Use Bright Colors to Signal Difficulty of Capture to Predators
Birds are able to recognize and learn to avoid attacking unpalatable, chemically defended butterflies after unpleasant experiences with them. It has also been suggested that birds learn to avoid prey that are efficient at escaping. This, however, remains poorly documented. Here, we argue that butterflies may utilize a variety of escape tactics against insectivorous birds and review evidence that birds avoid attacking butterflies that are hard to catch. We suggest that signaling difficulty of capture to predators is a widespread phenomenon in butterflies, and this ability may not be limited to palatable butterflies. The possibility that both palatable and unpalatable species signal difficulty of capture has not been fully explored, but helps explain the existence of aposematic coloration and escape mimicry in butterflies lacking defensive chemicals. This possibility may also change the role that putative Müllerian and Batesian mimics play in a variety of classical mimicry rings, thus opening new perspectives in the evolution of mimicry in butterflies.

作者討論的蝴蝶之一，摩爾福蝶。背面與腹面差異很大，其飛行行為讓人覺得很難追。 photo from Morpho menelaus (wiki)

文章中的範例之一，Parides anchises nephalion photo from Aluisio Ribeiro

credit Shutter stock

標題：Predator mimicry, not conspicuousness, explains the efficacy of butterfly eyespots

摘要

Large conspicuous eyespots on butterfly wings have been shown to deter predators. This has been traditionally explained by mimicry of vertebrate eyes, but recently the classic eye-mimicry hypothesis has been challenged. It is proposed that the conspicuousness of the eyespot, not mimicry, is what causes aversion due to sensory biases, neophobia or sensory overloads. We conducted an experiment to directly test whether the eye-mimicry or the conspicuousness hypothesis better explain eyespot efficacy. We used great tits (Parus major) as model predator, and tested their reaction towards animated images on a computer display. Birds were tested against images of butterflies without eyespots, with natural-looking eyespots, and manipulated spots with the same contrast but reduced resemblance to an eye, as well as images of predators (owls) with and without eyes. We found that mimetic eyespots were as effective as true eyes of owls and more efficient in eliciting an aversive response than modified, less mimetic but equally contrasting eyespots. We conclude that the eye-mimicry hypothesis explains our results better than the conspicuousness hypothesis and is thus likely to be an important mechanism behind the evolution of butterfly eyespots.

photo from Fig. 1

貓頭鷹蝶是常常用來解釋昆蟲眼紋的功用的例子，但是牠的眼紋到底是單純的眼紋還是跟真4的眼睛有一樣的功用，一直是個爭論不休的問題，加上前兩年有一篇文章說眼紋不是擬態眼睛，而單純是一種明顯的訊號，更讓貓頭鷹蝶的眼紋功用蒙上一層面紗。

photo from doublesex is a mimicry supergene

標題：The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations.


摘要

I review theoretical models for the evolution of supergenes in the cases of Bate- sian mimicry in butterflies, distylous plants and sex chromosomes. For each of these systems, I outline the genetic evidence that led to the proposal that they involve multiple genes that interact during ‘complex adaptations’, and at which the mutations involved are not unconditionally advantageous, but show advanta- ges that trade-off against some disadvantages. I describe recent molecular genetic studies of these systems and questions they raise about the evolution of sup- pressed recombination. Nonrecombining regions of sex chromosomes have long been known, but it is not yet fully understood why recombination suppression repeatedly evolved in systems in distantly related taxa, but does not always evolve. Recent studies of distylous plants are tending to support the existence of recom- bination-suppressed genome regions, which may include modest numbers of genes and resemble recently evolved sex-linked regions. For Batesian mimicry, however, molecular genetic work in two butterfly species suggests a new super- gene scenario, with a single gene mutating to produce initial adaptive pheno-types, perhaps followed by modifiers specifically refining and perfecting the new phenotype.

先說，這篇很難，完全在說分子生物學層級的機制。

作者整理有關貝氏擬態、性別決定與植物的二型花柱(distyly)討論基因重組與超基因的分子演化機制。這邊稍微整理貝氏擬態的部分，主要是談到有關這60年來藉由大鳳蝶 (Papilio memnon)、玉帶鳳蝶(P. polytes)與非洲白鳳蝶 (P. dardanus)的遺傳學與基因體學的研究，討論超基因如何出現的分子機制，如何透過基因重組的方式讓控制不同區域斑紋的基因逐漸在染色體上靠攏，作者整理兩個假說，說明兩個以上的擬態斑紋基因是如何出現在基因體內的兩種機制，分別是同染色體的調控與異染色體的調控（內文圖一）。這個整理對於擬態生物學關於分子層級的調控機制的研究提供一個統整性的框架。

未來將不再只是毒蝶內的穆氏擬態，貝氏擬態的背後神秘的作用機制也會越來越明朗。

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。

Multimodal defensive displays are commonplace, with prey combining conspicuous coloration, sounds, odours and other chemical emissions to deter predators. These components can signal to predators in multiple signal modalities to warn them that prey are defended. The aim of our review is to examine the form and function of multimodal warning displays. Data collected from the literature on multimodal insect warning displays show the degree of complexity and diversity that needs to be explained, and we identify patterns in the data that may be worthy of more rigorous investigation. We also provide a theoretical framework for the study of multimodal warning displays, and evaluate the evidence for different functional hypotheses that can explain their widespread evolution. Our review highlights that whilst multimodal warning displays are well documented, particularly in insects, we lack a good understanding of their function in natural predator–prey systems.

這篇落落長的review在討論的是為什麼有的物種同時具有警戒色，又有非視覺性的警戒機制，像是發出聲音、發出臭味等等，這是很有趣的一個問題，通常我們認為視覺的警戒訊號已經夠厲害，足以嚇阻捕食者，那為什麼又需要同時具有不同的非視覺訊號？如上圖中的細蝶 Acraea horta，是在本文中舉的其中一例，就同時具有視覺（橘紅色）、嗅覺（聞起來像瓢蟲）與味覺（會流出黃色汁液）。

本文主要分成三個部分，首先給了同時具有多項警戒機制的定義與出現在過往文獻的例子（主要是昆蟲），然後是定義如何判斷這些非視覺的訊號是警戒機制或次級防禦機制，最後提出這些非視覺的警戒訊號如何運作的假說以及這些訊號的分類。

對於警戒色的研究其實已經細緻到舌間上了，像是已經做到在吃到的一瞬間捕食者是否能判斷難吃然後學習起來之類的，雖然這種複合機制的討論並不是新梗，但相關的行為研究與眼化學研究的確是不多，大多數的討論都僅止於觀察與假設，因此這篇洋洋灑灑的回顧了一堆的例子，提出了一堆的假設，不僅是該團隊研究的新方向，也讓警戒性的研究多了一盞明燈。