Fig. 1 本研究定序的目標物種的分佈與其相關類群的親緣關係

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Fig. 2 a. 毒蝶染色體與家蠶染色體同源基因的比較圖，染色體間的連線代表同源基因的來源 b. 毒蝶化學感受蛋白與大樺斑蝶、家蠶間的關係，顯示出蝴蝶獨有與毒蝶獨有的擴張

Fig. 4 這個分析顯示控制擬態斑紋的基因座B/D的在族群間的基因交換證據

Fig. 1 基因入侵與祖先多態的兩個對立假設

摘要

Hybridization has the potential to transfer beneficial alleles across species boundaries, and there are a growing number of examples in which this has apparently occurred. Recent studies suggest that Heliconius butterflies have transferred wing pattern mimicry alleles between species via hybridiz- ation, but ancestral polymorphism could also produce a signature of shared ancestry around mimicry genes. To distinguish between these alternative hypotheses, we measured DNA sequence divergence around putatively introgressed mimicry loci and compared this with the rest of the genome. Our results reveal that putatively introgressed regions show strongly reduced sequence divergence between co-mimetic species, suggesting that their divergence times are younger than the rest of the genome. This is con- sistent with introgression and not ancestral variation. We further show that this signature of introgression occurs at sites throughout the genome, not just around mimicry genes.

Fig. 2 基因分化程度的比較

Fig. 1 實驗區域與實驗中所使用的表型 Hom. 同型合子 Het. 異型合子 exotic 非本地型

標題：Crossing fitness valleys: empirical estimation of a fitness landscape associated with polymorphic mimicry

摘要

Characterizing fitness landscapes associated with polymorphic adaptive traits enables investigation of mechanisms allowing transitions between fitness peaks. Here, we explore how natural selection can promote genetic mechanisms preventing heterozygous phenotypes from falling into non-adaptive valleys. Polymorphic mimicry is an ideal system to investigate such fitness landscapes, because the direction of selection acting on complex mimetic colour patterns can be predicted by the local mimetic community composition. Using more than 5000 artificial butterflies displaying colour patterns exhibited by the polymorphic Mullerian mimic Heliconius numata,we directly tested the
role of wild predators in shaping fitness landscapes.We compared predation rates on mimetic phenotypes (homozygotes at the supergene controlling colour pattern), intermediate phenotypes (heterozygotes), exotic morphs (absent from the local community) and palatable cryptic phenotypes. Exotic morphswere significantly more attacked than local morphs, highlighting predators’ discriminatory capacities. Overall, intermediates were attacked twice asmuch as local homozygotes, suggesting the existence of deep fitness valleys promoting strict dominance and reduced recombination between supergene alleles. By including information on predators’ colour perception, we also showed that protection on intermediates strongly depends on their phenotypic similarity to homozygous phenotypes and that ridges exist between similar phenotypes, which may facilitate divergence in colour patterns.

在先前的導讀中提到，控制穆氏擬態的毒蝶 (Heliconius) 斑紋基因的顯性性狀比較佔有優勢，中間型或隱性性狀能控制斑紋的機會相對減弱，而顯隱性與中間型又分別代表同型合子 (homozygous) 與異型合子 (heterozygous)，雖說遺傳結構支持顯性性狀比較容易表現，可這畢竟是實驗室內觀測到天擇的結果，在已經知道超基因的控制與顯隱性的優勢後，再次回到野外的話，這些斑紋的適存度 (fitness)又會有什麼樣的故事？

這篇研究就在討論我們已經知道穆氏擬態的毒蝶具有多態型，而且不同區域的多態型的遺傳結構各有不同，顯隱性表現也有各自的差異，但這是因為遺傳結構的限制，或是自然環境中天擇的影響，控制某些基因型的選汰還不清楚，在已經知道這麼多的基因體結構與其跟天擇連結的推測後，作者群再次把故事拉回野外實驗室中，測試天擇比較偏好同型或異型合子。

作者群依據Heliconius numata不同區域的型態，分別放置同型、中間型與非本地型的人工蝴蝶到野外環境中，總共放了超過5000隻的樣本到野外中，經過三天後回收樣本，檢查是否有U型或V型的攻擊痕跡，必且根據對應的形狀判斷是來自哪種捕食者的攻擊。

Fig. 2 不同表型的被攻擊次數，顯示中間型與非當地型被攻擊次數顯著較高 BB aa 同型合子 Ba 異型合子 exotic 非本地型

Fig. 3 不同表型在各種視覺模式下的關聯性

綜合各區域的結果顯示，同型合子個體受到的攻擊率顯著較低，異型合子（中間型）個體與非本地型的攻擊率顯著較高至同型合子的兩倍，支持這些斑紋的在不同場域的適存度有深度的分化。最後，若結合捕食者的視覺模型來看的話，發現中間型的適存度與當地的擬態型相似度有密切的關係，結合之前的研究來看，這個現象也會貢獻在斑紋的分化上。


<<相關閱讀>>

• 擬態蝴蝶的超基因(supergene)的顯性遺傳機制的演化
• 穆氏擬態的優勢斑紋演化的分子生物學機制
• 天擇在自然環境中如何正向篩選警戒訊號？

Heliconius numata的斑紋多樣性 photo: Keith. S. Brown Jr. (1979)

標題：Evolution of dominance mechanisms at a butterfly mimicry supergene

摘要

Genetic dominance in polymorphic loci may respond to selection; however, the evolution of dominance in complex traits remains a puzzle. We analyse dominance at a wing-patterning supergene controlling local mimicry polymorphism in the butterfly Heliconius numata. Supergene alleles are associated with chromosomal inversion polymorphism, defining ancestral versus derived alleles. Using controlled crosses and the new procedure, Colour Pattern Modelling, allowing whole-wing pattern comparisons, we estimate dominance coefficients between alleles. Here we show strict dominance in sympatry favouring mimicry and inconsistent dominance throughout the wing between alleles from distant populations. Furthermore, dominance among derived alleles is uncoordinated across wing-pattern elements, producing mosaic heterozygous patterns determined by a hierarchy in colour expression. By contrast, heterozygotes with an ancestral allele show complete, coordinated dominance of the derived allele, independently of colours. Therefore, distinct dominance mechanisms have evolved in association with supergene inversions, in response to strong selection on mimicry polymorphism.

photo: NSF

標題：Multilocus species trees show the recent adaptive radiation of the mimetic Heliconius butterflies

摘要

Müllerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification.We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.

說起毒蝶 (Heliconius)的故事，真是怎麼說也說不完，有關研究怎麼做也做不完。（文章也怎麼看都看不完.....）

早在大概二十世紀初的時候，一群研究毒蝶的科學家以當時的分子生物學技術，增幅幾個在粒腺體內的基因，重建毒蝶的演化歷史，終於得到一個長久以來疑問的證據：這些長的很像的毒蝶的親緣關係不是最近緣的，因此得知這些擬態的斑紋都是趨同演化來的。

Beltrán et al (2002) 以四個基因片段為基礎重建的親緣關係，包含25毒蝶屬物種與有關的外群

是不是近緣種這問題很重要嗎？試想，以普通的物種來說，有相似的斑紋或特徵代表牠們可能分類上是同一屬，同一科，或同一目，這個概念暗示相似特徵物種的親緣關係比較接近，很多類群的親緣關係結果也支持這個概念，這稱為系統發生學上的限制 (phylogenetic constrain)。那麼擬態的斑紋這麼像，雖然我們都假設這些斑紋是趨同演化來的，但在沒有證據的情況下，相似性可能來自牠們是近親的的原因也無法排除，直到系統發生學的結果出來後，才發現原來比我們想像的更複雜。

一開始就說，毒蝶的故事說也說不完，舊的議題配上新的技術是可以弄出新梗的。由於早年技術限制的問題，用的基因片段不多，種類也不多，只能看出個大概的輪廓，於是這個作者群重新檢驗毒蝶族 (Heliconiini) 的親緣關係，取樣了92%的物種以及22個基因，再次建立這個系統發生樹，並且輔以定年的資料，深入探討演化的歷史。

Fig. 1 本篇的主要結果，左下角為分化速率，越紅表示分化速率越快。作者同時將某些重要地理事件以紅線與雪花表示，並未與某些特定的節點產生關聯。

大方向的結果沒有改變，長的相似的依然不是姊妹群，分類上的結果支持一些稀有種分類上應該與某些常見種合併。透過這次全面性的取樣，作者群有機會測試兩個假說：毒蝶族的物種多樣性的分化，是因為過去兩千三百萬年的環境變遷，還是因為自身的演化速率的影響。在這個方面有了一個新的結論：整個族到了毒蝶屬的節上，似乎產生適應上的輻射演化 (adaptive radiation)，透過分化速度的分析，發現毒蝶屬的演化速度確實比起其他的節來說快，但這個速度是漸進的而非急速的 (rapid radiation)，而目前作者群無法明確的指出高度的分化是與哪個環境因子有明確的關聯。

毒蝶的故事，看起來還會繼續綿延下去，科學家的奮鬥將永不止息！

photo from Phillip's Natural World

標題：Beyond magic traits: Multimodal mating cues in Heliconius butterflies

摘要

Species coexistence involves the evolution of reproductive barriers opposing gene flow. Heliconius butterflies display colorful patterns affecting mate choice and survival through warning signaling and mimicry. These patterns are called “magic traits” for speciation because divergent natural selection may promote mimicry shifts in pattern whose role as mating cue facilitates reproductive isolation. By contrast, between comimetic species, natural selection promotes pattern convergence.We addressed whether visual convergence interferes with reproductive isolation by testing for sexual isolation between two closely related species with similar patterns, H. timareta thelxinoe and H. melpomene amaryllis. Experiments with models confirmed visual attraction based on wing phenotype, leading to indiscriminate approach. Nevertheless, mate choice experiments showed assortative mating. Mon- itoring male behavior toward live females revealed asymmetry in male preference, H. melpomene males courting both species equally while H. timareta males strongly preferred conspecifics. Experiments with hybrid males suggested an important genetic component for such asymmetry. Behavioral observations support a key role for short-distance cues in determining male choice in H. timareta. Scents extracts from wings and genitalia revealed interspecific divergence in chemical signatures, and hybrid female scent compositionwas significantly associatedwith courtship intensity by H. timareta males, providing candidate chemical mating cues involved in sexual isolation.

對於穆氏擬態的毒蝶 (Heliconius)來說，因為大家長的都很像（從人類的角度來）那麼這些那麼像的蝴蝶在找尋配偶的時候會不會弄錯呢？一些早期的研究指出毒蝶可經由視覺來挑選配偶，並且會偏好與自己比較相像的個體交配。比較近期（2000後）的一些研究也指出，雖然人類看起來很像的毒蝶，但不同種間的色素來源是不一樣的，因此會有些微妙的差異，而不同種毒蝶的視覺正好可以辨識這些差異，降低找錯配偶的機會。

可是實際上不知道為什麼，就是會有些種類只要有點像就交配，又有些種類似乎很忠誠，而基因體的研究又告訴我們不同種/亞種/族群可能會雜交，那麼究竟背後還有什麼因素，能讓某些種分辨跟自己同種的個體呢？

左為H. timareta ssp，右為H. melpomene amaryllis photo from La diversite des Heliconius

這個研究就在討論這個問題，究竟有什麼樣的因素會影響共域間擬態物種的種間隔離。實驗的概念基本上是利用兩種近緣的蝴蝶 H. timareta thelxinoe與H. melpomene amaryllis，透過雄性與雌性間的求偶行為觀察來得到結果。實驗的進行分為翅紋模型與費洛蒙分析兩個部分，除親代的純系實驗外，也執行兩者雜交後代的求偶偏好。實驗進行使用的雌性蝴蝶都是首次交配，確保沒有其他因子影響。

結果顯示H. melpomene的雄性會同時偏好兩者，但H. timareta則強烈的只偏好同種的個體，即使是雜交的雄性後代也同樣支持這樣的偏好。H. timareta的求偶行為觀察中發現，雄性要接近雌性到很短的距離才會決定交配與否。從翅膀與生殖器取出費洛蒙的分析顯示這兩種間的化學訊號顯著的不同。雜交的雌性後代的費洛蒙組成明顯的會吸引H. timareta。這樣的結果支持除了透過視覺外，費洛蒙也扮演重要的角色。

雖然說鱗翅目昆蟲有複合式的求偶與種間辨識訊號也不是什麼大新聞，但透過遺傳學、化學生態學、行為學與生物統計學各種工具來更深入解析已知的資訊，這種跨界分析近來也成為討論擬態各種問題的趨勢。

photo from The magic of life butterfly house

標題：Molecular mechanisms of dominance evolution in Müllerian mimicry.

摘要

Natural selection acting on dominance between adaptive alleles at polymorphic loci can be sufficiently strong for dominance to evolve. However, the molecular mechanisms underlying such evolution are generally unknown. Here, using Müllerian mimicry as a case-study for adaptive morphological variation, we present a theoretical analysis of the invasion of dominance modifiers altering gene expression through different molecular mechanisms. Toxic species involved in Müllerian mimicry exhibit warning coloration, and converge morphologically with other toxic species of the local community, due to positive frequency-dependent selection acting on these colorations. Polymorphism in warning coloration may be maintained by migration–selection balance with fine scale spatial heterogeneity. We modeled a dominance modifier locus altering the expression of the warning coloration locus, targeting one or several alleles, acting in cis or trans, and either enhancing or repressing expression. We confirmed that dominance could evolve when balanced polymorphism was maintained at the color locus. Dominance evolution could result from modifiers enhancing one allele specifically, irrespective of their linkage with the targeted locus. Nonspecific enhancers could also persist in populations, at frequencies tightly depending on their linkage with the targeted locus. Altogether, our results identify which mechanisms of expression alteration could lead to dominance evolution in polymorphic mimicry.

根據很多對於擬態的觀測與研究結果，無庸置疑的這是一個天擇的結果，但科學家無論如何觀測，從野外的族群到細胞裡的基因體，都只能觀測到這些結果，與推測可能的原因，對於天擇實際上透過什麼樣的「工具」來留下有優勢的斑紋，至今仍然是個很大的謎團。

文章中基礎的方程式(1)與(2)式

這個研究透過數學模型，模擬分子生物學中的調節子 (modifier) 如何作用在控制顏色斑紋的基因上。方程式中假設不同族群的多態型能夠透過族群某種比例的遷徙交換基因，在不同的族群就會產生不同的斑紋，進而模擬天擇是如何透過調節子來留下具有優勢的基因。方程式的展開與建構很複雜就姑且不提，總之是透過考量了優勢參數、突變、毒性程度、族群遷徙、基因重組率與捕食者的認知等等參數建構出的數學模型。結果發現具有優勢的斑紋能夠透過顏色基因的多態型平衡來達成。這個優勢的演化能夠從調節子來增強某個特殊的基因，無論這個基因是否與某個特殊的基因在同一條染色體上。

總之，這篇實在太抽象了，有興趣或有需要的朋友請自行詳細研讀吧。

photo from Heliconius.org

photo from Kronforst Lab

標題：Wing patterning genes and coevolution of Müllerian mimicry in Heliconius butterflies: Support from phylogeography, cophylogeny, and divergence times.

摘要

Examples of long-term coevolution are rare among free-living organisms. Mullerian mimicry in Heliconius butterflies had been suggested as a key example of coevolution by early genetic studies. However, research over the last two decades has been dominated by the idea that the best-studied comimics, H. erato and H. melpomene, did not coevolve at all. Recently sequenced genes associated with wing color pattern phenotype offer a new opportunity to resolve this controversy. Here, we test the hypothesis of coevolution between H. erato and H. melpomene using Bayesian multilocus analysis of five color pattern genes and five neutral genetic markers.We first explore the extent of phylogenetic agreement versus conflict between the different genes. Coevolution is then tested against three aspects of the mimicry diversifications: phylogenetic branching patterns, divergence times, and, for the first time, phylogeographic histories.We show that all three lines of evidence are compatible with strict coevolution of the diverse mimicry wing patterns, contrary to some recent suggestions. Instead, these findings tally with a coevolutionary diversification driven primarily by the ecological force of Mullerian mimicry.

穆氏擬態的毒蝶(Heliconius)就是很像又都有毒，這麼相像的斑紋到底怎麼來的？這是一個很大的疑問。而且，很多人認為兩個物種長的這麼像又分佈在同一個地方，承受一樣的天擇壓力，那麼，這個斑紋應該是共演化(coevolution)的關係吧？

大約十幾年前時有James Mallet有寫文章特別討論過，那個時候特別提到，雖然毒蝶的每個斑紋都很像，但這僅是斑紋上的趨同，不是兩個物種的共演化。然而在這十年間，分子生物技術的發展大量應用在毒蝶擬態的研究上，無論是控制斑紋的基因，或是與種化有關的基因都被找出來了，如果重新檢視有沒有共演化這個問題，會不會不一樣呢？

於是H. erato 與H. melpomene這兩個經典的穆氏擬態分類群又上場了。作者利用了五個控制斑紋的基因 (optix, bves, kinesin, GPCR, and VanGogh)跟五個中性基因 (COI and COII, plus four nuclear genes: SUMO, Suz12, 2654, and CAT)再次重建親緣關係。作者透過比較兩個物種的親緣關係的樹型、分化的時間與生物地理的演化歷史，重新分析這兩個物種的演化歷史。結果發現這兩個物種在這三方面的分析中都支持兩者間的共演化關係，樹型相似、斑紋分化時間相似，生物地理的分析也相關，這個結果似乎提供了一個與之前完全相反的證據，支持新熱帶蝴蝶的擬態斑紋的共演化。

這個文章有另一個值得討論的地方，以前總認為控制擬態的斑紋，或是說明顯受到天擇/性擇的基因，是不能用來重建物種的親緣關係，因為會有無法正確反應物種演化歷程的疑慮，因此總是會選擇被天擇/性擇影響比較小，比較「中性」的基因來重建親緣關係，可是這個文章用了應該明顯受到天擇影響的基因，反而呈現了完全不同的理論與故事，這給研究演化的科學家們一個新的思考方向，或許使用以前不被考慮的基因，更能反應該性狀的演化歷程。

photo from Fig. 1

標題：Warning signals are under positive frequency-dependent selection in nature.

摘要

Positive frequency-dependent selection (FDS) is a selection regime where the fitness of a phenotype increases with its frequency, and it is thought to underlie important adaptive strategies resting on signaling and communication. However, whether and how positive FDS truly operates in nature remains unknown, which hampers our understanding of signal diversity. Here, we test for positive FDS operating on the warning color patterns of chemically defended butterflies forming multiple coexisting mimicry assemblages in the Amazon. Using malleable prey models placed in localities showing differences in the relative frequencies of warningly colored prey, we demonstrate that the efficiency of a warning signal increases steadily with its local frequency in the natural community, up to a threshold where protection stabilizes. The shape of this relationship is consistent with the direct effect of the local abundance of each warning signal on the corresponding avoidance knowledge of the local predator community. This relationship, which differs from purifying selection acting on each mimetic pattern, indicates that predator knowledge, integrated over the entire community, is saturated only for the most common warning signals. In contrast, among the well-established warning signals present in local prey assemblages, most are incompletely known to local predators and enjoy incomplete protection. This incomplete predator knowledge should generate strong benefits to life history traits that enhance warning efficiency by increasing the effective frequency of prey visible to predators. Strategies such as gregariousness or niche convergence between comimics may therefore readily evolve through their effects on predator knowledge and warning efficiency.

photo from Fig. S1

面對擬態這個自然現象時，科學家都會說「因為同享這個斑紋的物種被捕食者避免，所以擬態斑紋是天擇後留下來的結果」，也就是說，天擇偏好牠們，所以留下來了，可是其實只有很片面的證據支持，有的時候是實驗室內的行為實驗，有的時候是區域性的生態觀察，所以「天擇偏好擬態的性狀」這件事其實是結果，科學家對天擇如何偏好這樣的性狀知道的還很少。

秘魯北方的數個區域的毒蝶(Heliconius)提供研究這個假說的環境。作者利用1997-2013年的採集資料判斷出幾個區域，這幾個區域的毒蝶（見上圖一）佔優勢的擬態型都不盡相同，而且每個區域佔優勢的型每年出現的頻率都很穩定。作者測試如果有其他的擬態型出現在當地的話，應該會被捕食者所篩選的假設，利用製作非常精巧的人工假餌（印製精確，經過測試反射光譜與套用捕食者模型後，知道看起來可能的模樣），在各地區設置6-8公里的穿越線，放置480-600個假餌（120/型，4-5型/區域）。

photo from fig. 2

結果顯示如果不是當地佔優勢的擬態型，被攻擊的頻率就是會比較高（圖二）。但有趣的是不佔優勢的擬態型不會無限制的被攻擊，而是會被攻擊到與當地不佔優勢的擬態型的比例相當。這也就是說當地捕食者的篩選不是只針對某個型，而是基於全面性的「知識」判斷能不能吃。而那些看起來跟優勢型相像的也某種程度上受到保護，這可能會因為捕食者的「知識」不足而有機會發展成為優勢族群。

這整個實驗展示天擇如何在擬態上展現「正向選汰」的機制，實驗本身不難，珍貴的是那1997-2013的採集資料，若非有這些基礎資料，連判斷擬態型的區域都極為困難，更別提當地的各型所佔的比例，也凸顯長期樣區的物種記錄基礎研究的重要性。

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.

標題：Mimicry refinement: Phenotypic variations tracking the local optimum [pdf]

摘要

1.Müllerian mimicry between chemically defended preys is a textbook example of natural selection favouring phenotypic convergence onto a shared warning signal. Studies of mimicry have concentrated on deciphering the ecological and genetic underpinnings of dramatic switches in mimicry association, producing a well-known mosaic distribution of mimicry patterns across geography. However, little is known about the accuracy of resemblance between natural co-mimics when the local phenotypic optimum varies.

2.In this study, using analyses of wing shape, pattern and hue, we quantify multimodal phenotypic similarity between butterfly co-mimics sharing the so-called postman pattern in different localities with varying species composition.

3.We show that subtle but consistent variation between populations of the localised species, Heliconius timareta thelxinoe, enhance resemblance to the abundant co-mimics which drive the mimicry in each locality.

4.Those results suggest that rarer co-mimics track the changes in the phenotypic optimum caused by gradual changes in the composition of the mimicry community, providing insights into the process by which intra-specific diversity of mimetic pattern may arise. Furthermore, our results suggest a multimodal evolution of similarity, with coordinated convergence in different features of the phenotype such as wing outline, pattern and hue.

5.Finally, multilocus genotyping allows estimating local hybridization rates between H. timareta and co-mimic H. melpomene in different populations, raising the hypothesis that mimicry refinement between closely-related co-mimics may be enhanced by adaptive introgression at loci modifying the accuracy of resemblance.
無論從哪個角度來說，穆氏擬態群內的斑紋應該要越相似越好，如果有個體長的突然與大家不一樣，可能就會被天擇排擠消失，也或許有機會獨樹一格（低機率），雖然人類視覺角度來看，穆氏擬態群的每個物種或個體都十分相似，但之前已經有研究指出不同種間的相似斑紋來源可能是透過不同的基因調控來的，若是如此，自然界中展現出來的表型看起來雖然一致，但會不會是在某個可接受的誤差範圍內呢？

這篇研究討論毒蝶的一個稱做「郵差」(postman)的擬態型，參與這個擬態型的物種有H. melpomene, H. timareta, H. erato, H. timareta, H. telesiphe，之所以會有這樣的考量在於其中有個共擬態亞種H. timareta thelxinoe在兩個區域的族群有些微的變化，而這兩地的model也剛好有這樣的不同。作者測量這些蝴蝶的翅型、翅紋樣式與色調來比較這兩個族群間的差異是否一致。結果顯示H. timareta thelxinoe的斑紋在兩地間有連續性的變化，支持穆氏擬態中斑紋應該與當地的model趨近的觀點。

這也是個model強烈的主導mimic的斑紋變化，在天擇的作用下，mimic透過細微的改變趨近model的一證據。（自然界中的霸凌？）

標題：Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling

摘要

An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.

標題：A bird's eye view of two mimetic tropical butterflies: coloration matches predator's sensitivity

摘要

Unprofitable prey with conspicuous warning signals are often mimicked by other species, which then gain protection from predators. How closely two mimetic spe- cies resemble one another depends upon the visual perception of the signal recei- ver. However, most studies of mimetic coloration have been conducted using only the human visual system, which differs greatly from that of most animals. To bet- ter understand mimicry, we should study mimetic visual signals through the eyes of the intended receiver. Here, we use avian visual models to test predictions of putative Batesian mimicry in two Amazonian butterflies, Mimoides pausanias and Heliconius sara. We calculated Just Noticeable Differences (JNDs) and tetrahedral color volumes for 11 different patches: iridescent blue, yellow bars, red spots and black background. Several color patches were not visually discriminable for both avian visual systems (UV/VIS and V/VIS), and visual discrimination (i.e. degree of mimicry) of color patches depended upon the avian visual system. These two but- terfly species are more mimetic when viewed by their likely avian predators, which have V/VIS vision. Therefore, this mimetic assemblage may have evolved to be more spectrally accurate in the non-UV wavelengths which their avian predators are able to see. However, while many color patches of the two species were mod- eled to be difficult to discriminate, most color patches were not perfect matches regardless of visual system, and several patches were very poor mimics. Through this study we demonstrate the importance of testing putative mimetic assemblages using known predator perceptual models and lay a foundation for behavioral studies to further test mimicry in H. sara and M. pausanius.

摘要 [原文網址]

The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red color-pattern variation. We found that although unlinked genes partition populations by geographic region,optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80–250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.

在系統發生學中，如果我們想要知道一個特徵的演化起源，也就是大家最想看的「怎麼演化」，通常會有個樹，上面有很多顏色很漂亮，然後你追著那個你想看的顏色，就會知道這個特徵發生了幾次，然後你在看圖說故事（譬如多年前有人探討竹節蟲翅的演化來源一樣）。重點就在於通常我們重建一棵樹的時候，理論告訴我們要選中性或偏中性的分子標記，不能選那些受到強烈天擇作用的標記，這樣才能純粹的反應物種間的關係，然後再用你想看的特徵去追溯，才會知道演化的來源。

而這如果用在擬態的演化這件事上會怎樣？通常你會看到不同擬態樣子的物種混在同一個支系裡，然後你用這個樹去追溯擬態的特徵，九成九會告訴你「所有的擬態特徵都是每個物種獨立演化多次來的」，所以哪個特徵先出現會變得模糊不清，原因就在於這些中性的分子標記是可以在各個物種間傳來傳去的，不一定會跟著強烈天擇的翅紋走，因此基於這些標記重建的樹無法反應擬態特徵的演化歷史。

所以為了知道這個特徵的演化來源與方向，這篇文章就用了控制斑紋的基因重建親緣關係，結果發現不同物種間但同樣斑紋的種類親緣關係較近，也就是在分子的層級上，擁有相同擬態翅紋的物種是趨同的，這就可以用來解釋很多事情，像是提供穆氏擬態的演化假說證據（註）等等。

當然要做到這個層級的前提有很多，像是要先知道各個控制斑紋的基因是哪個，先花大錢把序列全部定出來，實驗動物本身要能夠雜交容易飼養繁殖等等，相較於其他地區的擬態群來說，毒蝶提供很多這類的優勢，自然是個很好的模式動物。

註：穆氏擬態的演化假說是不同物種間的斑紋會越來越像，以求達最適化。

The colorful wing patterns of Heliconius butterflies represent an excellent system in which to study the genetic and developmental control of adaptation and convergence. Using qRT-PCR and in situ hybridization on developing wings of the co-mimic species Heliconius melpomene andHeliconius erato, we have profiled the expression of three candidate genes located in the genomic locus controlling red color pattern variation. We found convergent domains of gene expression in H. melpomene and H. erato associated with red wing elements in the two genes optix andkinesin. During early pupal development of both species, the expression of optix perfectly associated with all red pattern elements whereas that of kinesin was specifically correlated with the presence of the red forewing band. These results provide evidence for the use of these two tightly linked patterning genes, acting together to create convergent wing phenotypes in Heliconius and constituting a hotspot of adaptation.

毒蝶的擬態斑紋是已經知道由一個supergene所調控，而這個supergene的序列也大致上已經定序完成，哪個基因與哪個斑紋的連結也大致清楚，但其中基因相對表現，或如何表現的資料還不是太多。這個文章討論兩個共擬態的毒蝶H. melpomene與H. erato的演化發育基因如何調控擬態的斑紋，這類的毒蝶的擬態斑紋有幾個主要的類型，主要是翅上紅色與黃色的斑紋與表現，稍微有一些不一樣就會被天擇掉，或是被認為加入另一個擬態群。

文中找出了三個可能調控斑紋的基因，分別是optix, kinesin與bves，結果發現兩種蝴蝶中，在蛹的早期，optix與所有紅色的斑紋表現都有關，而kinesin只與後翅的紅色斑紋有關，bve則表現量不高，或與這個擬態斑紋的表現關連性較低。