photo from Aposematism (wiki)

標題：Are aposematic signals honest? A review

摘要

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.

從以前的自然學家發現警戒性並且描述這個現象以來，我們對於一個物種有警戒色總是假設「有明顯的訊號，而且有危險的防禦機制」的這個前提，來假設所有警戒性的物種都是這樣，可是，如果有物種其實只有警戒性，但是沒有任何防禦機制，這時就會說這個訊號「不誠實」。會有這個疑慮就是因為有的物種本身長得很誇張（例如有很多刺），這就毫無疑問的展現其防禦，但有的物種必須要攻擊後才知道（例如珊瑚蛇），這時中間很多假設與疑問就出現了。

基本上，警戒性分為「訊號」與「防禦」，就演化歷程來說， 無論哪種特徵的出現都必須有相當的「花費」(cost)，如果先演化出了訊號很有用，那麼還會需要在花費更多的力氣出現防禦嗎？如果這訊號反而吸引攻擊，那不就白花這些能量？因此也有科學家的看法認為警戒性本身是種「殘障」，不管做什麼都受限，而且必須花費巨大的演化機會投資在警戒性的演化上。

這篇回顧就在討論警戒性到底是不是確實的反應物種的防禦，以及從博奕理論(game theory)的觀點，辯證物種在警戒性的演化上的花費與收穫的平衡，最後加上實際研究過的例子（箭毒蛙與無脊椎動物）來佐證，整理上來說篇幅雖然很長，但讀完能對警戒性的演化有更進階的概念。

photo from Amateru Entomologists' Society

標題：Evolving détente: the origin of warning signals via concurrent reciprocal selection.

摘要

Casualties and impediments inflicted on consumers by defended prey, and vice versa, may be averted by vocalizations, postures, coloration, scents, and other warning, or so-called aposematic, displays. The existence of aposematic signals has challenged biologists who have sought plausible mechanisms for their evolution. Here, we elaborate on the rationale for the hypothesis that aposematic signals arise via concurrent reciprocal selection (CRS) enacted between inimical signal receivers and signal emitters, where signal emitters, e.g., defended prey, select against non-discriminating signal receivers, e.g., predators, and signal receivers select against unrecognized signal emitters. It is postulated that this mutual selective interaction culminates in the survival of discriminating signal receivers that avoid signal emitters, and recognized (distinctive) signal emitters that are avoided by signal receivers. A CRS hypothesis for the evolution of aposematism, therefore, maintains that distinctive features of prey arise in response to selection imposed by consumers, and that avoidances of those features by consumers arise in response to selection imposed by defended prey. We discuss the plausible inception of aposematism via CRS in light of related hypotheses, and describe points of concordance with previous observations and suggestions on the origin of aposematism. Aposematism arising via CRS is not contingent upon the relatedness of signallers, aversions acquired by learning, or other conditions postulated for some other evolutionary hypotheses. CRS is a credible alternative hypothesis for the evolution of warning signals in diverse consumer-prey interactions.

關於警戒色演化上怎麼冒出來的一直是件很奇怪的事。簡單的說，一個物種如果變的顯眼但能吃，捕食者很快就發現這能吃；反過來， 如果物種變的顯眼前先變的不能吃，那麼捕食者學的起來嗎？還是連結的是變顯眼前的顏色？如果這樣還需要的顯眼嗎？還要考慮各種捕食者與被捕食者間的因子與連結，造就各式各樣的對於警戒色演化上的假設，但各自有道理，到現在也沒個定論。

這篇文章整理了一個整合訊號接收者與訊號發出者間關係的理論，稱為concurrent reciprocal selection (CRS)，大致上是說不管是從哪個角色出發，發出訊號者會傾向留下能認得訊號的接收者，認不得的會被篩選掉，而接收者會傾向把能辨識的發出者留下，分不出來或難以辨識的會被篩選掉，形成一個同時間互相篩選協調的機制。（細節詳見內文）

CRS對警戒色的演化理論示意圖 photo from Fig. 1

通常理論發展出來，大多是單方面的對訊號發出者篩選，變化也是發出者在變化，可是這篇加入訊號接收者在選汰上的角色，而非單純討論哪些心理因子可能對演化有影響，而是認為這是一個雙向的機制，的確是與先前發展的理論不盡相同。這個理論聽起來當然也是很理想（每個理論看起來都很理想），也提供我們對於警戒性的演化新的思考方向。

有機會來整理一下所有關於警戒色演化的理論好了。

photo from dailymail

標題：Cognition and the evolution of camouflage

摘要

Camouflage is one of the most widespread forms of anti-predator defence and prevents prey individuals from being detected or correctly recognized by would-be predators. Over the past decade, there has been a resurgence of interest in both the evolution of prey camouflage patterns, and in under- standing animal cognition in a more ecological context. However, these fields rarely collide, and the role of cognition in the evolution of camouflage is poorly understood. Here, we review what we currently know about the role of both predator and prey cognition in the evolution of prey camouflage, outline why cognition may be an important selective pressure driving the evolution of camouflage and consider how studying the cognitive processes of animals may prove to be a useful tool to study the evolution of camouflage, and vice versa. In doing so, we highlight that we still have a lot to learn about the role of cognition in the evolution of camouflage and identify a number of avenues for future research.

photo from wohinauswandern

隱蔽與偽裝一直是科普教材的最愛，放一張圖片讓大家來尋找目標物種在哪裡，體驗生物體色的驚奇變化，讚嘆為何能如此躲過大家的視線，必然也能躲過野外的眾多天敵。姑且不論隱蔽、偽裝與擬態在定義上的分野（很多文章會把這些名詞混為一談，但這其實不容易弄清，科學家們也吵過架，日後我會發專文詳談各名詞的定義與使用），光是上述所說的狀況，就是讓人類扮演捕食者的角色，尋找自己的獵物，而當你面對這樣的圖片時會有什麼反應？仔細的慢慢尋找？快速的搜尋？如果找到一次，第二次是否更容易找到？

這些想法與認知都可能出現在野外的捕食者，而野外的這些生物面對的是更嚴酷的三維空間的搜尋，以及路過就沒得吃會餓死的壓力，反過來說，獵物所經歷的就是一旦被發現就可能喪命的風險。

因此認知行為必然在偽裝/隱蔽的演化上扮演重要的角色，但是究竟如何運作，捕食者實際上會做出什麼行為，在這篇文章中整理了近十年來用認知行為學的方式進行測試，通常是以家雞與Opisthograptis luteolata的幼蟲（尺蛾科）進行實驗。現在已經知道當捕食者沒經驗的時候會傻傻的把枝條當成可以吃的，但經歷過之後就會放慢攻擊的速度，似乎有某種程度的判斷。

Opisthograptis luteolata 幼蟲 photo from http://www.fredmiranda.com/forum/topic/1250262

捕食者判斷這類的獵物時，有很大部分依賴自身經驗所產生的搜索印記 (searching image)，也就是說必須經歷過才能對獵物產生選汰壓力。那麼對於實際上是否有夠多的個體有這樣的經歷，或是能透過社會性的交流來學習，我們都還不知道，對於這些關鍵還需要更多未來的研究才能揭開迷團。

這可以從下圖來說明：
這是一個測試，將鳥分成兩組，其中一組只給單一隱蔽性獵物（實線），另一組給兩種隱蔽性獵物（虛線），分別各給10個測試，1次測試連續呈現20次獵物。左圖說明無論是經歷一種或兩種，捕食者的學習速度會呈現漸進線的曲線（就是會趨近一個數值，而不會無止盡的上升或下降），右圖呈現的是當鳥同時面對兩種獵物時，搜索印記似乎很難產生。結果就是捕食者面對越多種隱蔽/偽裝獵物時，就更難注意到原來有這樣的東西可以吃，這個忽略就讓隱蔽/偽裝的獵物有演化的空間。而對捕食者來說，就是會忽略這樣的獵物

photo from Fig. 1

即使如此，作者也不停強調，我們對於這樣的認知還是知道的太少，但瞭解捕食者的認知行為的確有助於推測這種性狀的演化。

photo from fig.1

標題：Learning about aposematic prey

摘要

The question, “Why should prey advertise their presence to predators using warning coloration?” has been asked for over 150 years. It is now widely acknowledged that defended prey use conspicuous or distinctive colors to advertise their toxicity to would-be predators: a defensive strategy known as aposematism. One of the main approaches to understanding the ecology and evolution of aposematism and mimicry (where species share the same color pattern) has been to study how naive predators learn to associate prey’s visual signals with the noxious effects of their toxins. However, learning to associate a warning signal with a defense is only one aspect of what predators need to do to enable them to make adaptive foraging decisions when faced with aposematic prey and their mimics. The aim of our review is to promote the view that predators do not simply learn to avoid aposematic prey, but rather make adaptive decisions about both when to gather information about defended prey and when to include them in their diets. In doing so, we reveal what surprisingly little we know about what predators learn about aposematic prey and how they use that information when foraging. We highlight how a better understanding of predator cognition could advance theoretical and empirical work in the field

以往對於捕食者面對警戒性的人類的認知，就是捕食者會「避免」攻擊這樣的食物，而且應該會把這樣的獵物完全排除在牠們的菜單之內。然而近來的某些理論與實驗支持捕食者會把某些不好吃的獵物也列入可食用清單裡，這讓動物行為學家重新思考捕食者在面對有警戒性的獵物時，可能不會只是單純的學到「避免」，而是全面性的思考與學習何時可以吃，怎樣的獵物可以偶爾吃，什麼完全不能吃。

這篇回顧整理了這幾年行為科學家的想法與實驗，從思考捕食者如何避免，到思考捕食者如何適應性學習，而這樣思考的轉變又影響行為學在斑紋演化與生態作用機制的實驗設計與討論，讓科學家在連結捕食者與獵物間的角色有了未來的研究方向。

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。

Wing-pattern mimicry in butterflies has provided an important example of adaptation since Charles Darwin and Alfred Russell Wallace proposed evolution by natural selection .150 years ago. The neotropical butterfly genus Heliconius played a central role in the development of mimicry theory and has since been studied extensively in the context of ecology and population biology, behavior, and mimicry genetics. Heliconius species are notable for their diverse color patterns, and previous crossing experiments revealed that much of this variation is controlled by a small number of large-effect, Mendelian switch loci. Recent comparative analyses have shown that the same switch loci control wing-pattern diversity throughout the genus, and a number of these have now been positionally cloned. Using a combination of comparative genetic mapping, association tests, and gene expression analyses, variation in red wing patterning throughout Heliconius has been traced back to the action of the transcription factor optix. Similarly, the signaling ligand WntA has been shown to control variation in melanin patterning across Heliconius and other butterflies. Our understanding of the molecular basis of Heliconius mimicry is now providing important insights into a variety of additional evolutionary phenomena, including the origin of supergenes, the interplay between constraint and evolvability, the genetic basis of convergence, the potential for introgression to facilitate adaptation, the mechanisms of hybrid speciation in animals, and the process of ecological speciation.

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。

原文標題：Lepidopteran wing patterns and the evolution of satyric mimicry

摘要 [原文網址]

The hypothesis of satyric mimicry postulates that the colour patterns of an animal may make its identity ambiguous, and this ambiguity interferes with the process of perception in vertebrate predators for a sufficient time to allow the potential prey to take evasive action. It has now been found that eyespots and other designs on the wings of many insect species are often coupled with other wing patterns and designs. These composite images often closely resemble heads and bodies of vertebrates (including birds and reptiles) and of various invertebrates. Such images can be perceived in living insects, although only rarely in set specimens because of displacement of the components. Visual processing by non-mammalian vertebrates generally involves attention to detail, suggesting that, at least initially, and unlike humans, they perceive embedded images on insect wings and bodies and ignore the whole or Gestalt. They are therefore likely to be confused by the ambiguity of the potential prey. It can be calculated that a delay of the order of only tenths of a second in the attack on a stationary insect by a predator could result in failure of capture. It is proposed in the present review that the concept of satyric mimicry be extended to include complex imagery of other organisms. Such iconic images, which often represent toxic or dangerous animals, are particularly common amongst saturniid moths and nymphalid and danaid butterflies (including the Monarch butterfly, Danaus plexippus). © 2013 The Linnean Society of London

這篇主要是在討論satyric mimicry這件事情，特別歸納了有關鱗翅目的相關研究，包含如何作用，不同類型捕食者的反應等。那麼，首要的問題應該是要先解釋什麼是satyric mimicry。

Satyric mimicry包含的擬態類型像是假頭假眼，或是像食蚜蠅這種不太像的擬態，都可以算是。首次被定義是在Howse & Allen (1994)這篇文章，意指「有點像什麼又不太像什麼」的不完美擬態，對於這個名詞目前找不到一個很好的翻譯，satyric這個字查到的意思都是性好酒色的(adj.)(明顯的跟這件事沒關係)，因此要給個中文名稱，或許可稱為「模稜兩可的擬態」。這個故事要從Dittrich et al (1993)的故事說起，這篇文章中用鴿子與食蚜蠅測試不完美擬態的實驗中，發現了鴿子可以分辨很像跟很不像的食蚜蠅，可是中間那些有點像又有點不像似乎就不太能分辨，可是鴿子對於這些東西的分辨時間變長了，因此Howse & Allen (1994)就認為這些不太像的擬態是「故意」的，用意在拖長捕食者的分辨時間，也就是增加自己的逃跑時間。

雖然這個理論被建立，但也不是每個人都同意。像是Sherratt (2002)中提到他認為satyric mimicry並不存在的一個原因是這個理論建立在族群的頻度上，但是不完美擬態的每個型頻度都不高，因此一個模稜兩可且頻度不高的斑紋是不太可能從天擇中存活下來的，而另一個可能是這些斑紋與擬態無關，單純的只是顯示牠們也不可食。

總之這些理論都還沒個結局，尤其是這種不完美擬態為什麼能夠存在，依然值得討論。

原文標題：Evolution of diversity in warning color and mimicry: polymorphism, shifting balance, and speciation

摘要 [原文網址]
Mimicry and warning color are highly paradoxical adaptations. Color patterns in both Müllerian and Batesian mimicry are often determined by relatively few pattern-regulating loci with major effects. Many of these loci are “supergenes,” consisting of multiple, tightly linked epistatic elements. On the one hand, strong purifying selection on these genes must explain accurate resemblance (a reduction of morphological diversity between species), as well as monomorphic color patterns within species. On the other hand, mimicry has diversified at every taxonomic level; warning color has evolved from cryptic patterns, and there are mimetic polymorphisms within species, multiple color patterns in different geographic races of the same species, mimetic differences between sister species, and multiple mimicry rings within local communities. These contrasting patterns can be explained, in part, by the shape of a “number-dependent” selection function first modeled by Fritz Müller in 1879: Purifying selection against any warning-colored morph is very strong when that morph is rare, but becomes weak in a broad basin of intermediate frequencies, allowing opportunities for polymorphisms and genetic drift. This Müllerian explanation, however, makes unstated assumptions about predator learning and forgetting which have recently been challenged. Today's “receiver psychology” models predict that classical Müllerian mimicry could be much rarer than believed previously, and that “quasi-Batesian mimicry,” a new type of mimicry intermediate between Müllerian and Batesian, could be common. However, the new receiver psychology theory is untested, and indeed it seems to us unlikely; alternative assumptions could easily lead to a more traditional Müllerian/Batesian mimicry divide.



這篇文章的出現，綜合了近100年內發展的擬態理論，解釋擬態與警戒色的形成與演化。


擬態群對於演化學家而言，是件令人驚奇，卻又難以解釋的現象，雖然早在十八世紀就已提出這個現象的解釋，但至今仍然無法以一個全面的結果，說明這個現象如何形成，因此在不同領域的生物學家各持己見，因為沒人真的看到這個現象如何形成，有人用數學模型模擬幾萬個世代，推測斑紋的變化；有人從實驗行為學的角度，測試天擇對於擬態性狀的生成；有人從遺傳學的角度，測得擬態物種間的差異與性狀的變化，但無論哪個領域，都無法完美的解釋擬態的產生，當A理論在A領域生成時，在B領域就無法成立。這篇文章就概括所有領域的理論，提出對於現在擬態生物學的看法。


其中比較不一樣的地方在於，作者表達對於quasi-Batesian mimicry與Mullerian mimicry的看法，他們認為如果不在frequency-dependent 的前提下，只藉著receiver psychology是難以解釋擬態物種多態型的形成，也可能會失去擬態的多樣性，也就是不會有像目前看到這麼多樣化的擬態群，而是會趨於簡單化，就算可食度不同，仍然要回到捕食者是否能遇到這個不好吃的東西，仍然回到frequency-dependent的假設下，大大的質疑quasi-Batesian mimicry的可信度。


雖然如此，quasi-Batesian mimicry仍然無法被推翻，因為我們對於捕食者的反應仍了解的太少，有時甚至無法確定何為捕食者，因此理論跟行為學家對於這樣的推論仍然繼續提出證據，爭論依舊沒有結束。