獵物群落結構影響捕食者對於穆氏擬態之選擇

Ihalainen E, Rowland HM, Speed MP, Ruxton GD, Mappes J. 2012 Prey community structure affects how predators select for Mullerian mimicry. Proc Biol Sci. DOI:10.1098/rspb.2011.2360 [Full]

Keywords: aposematism; avoidance learning; Batesian mimicry; generalization

當不可食的獵物越多時，是否會分散捕食風險?

[圖片來源]

Rowland HM, Wiley E, Ruxton GD, Mappes J & Speed MP. (2010) When more is less: the fitness consequences of predators attacking more unpalatable prey when more are presented. Biol. Lett. 6: 732-735. doi: 10.1098/rsbl.2010.0207 [Full text]

1879年，Fritz Müller提出：在擬態行為中，當具警戒信號的獵物比例增加時，獵物的被捕食風險將會降低，因此作者以110隻雄性小雞(Gallus gallus domesticus)作為捕食者，以麵包屑加水作為人工獵物，以chloroquine phosphate作為苦味劑，並且將人工獵物進行染色，可食的(edible)為綠色，不可食的(unpalatable)為紅色，再改變不可食人工獵物的數量，檢示當不可食獵物增加時是否改變捕食風險。結果發現，當不可食獵物數量增加時(總獵物量增加)，捕食者攻擊不可食獵物的次數也增加，因此不可食獵物的數量會下降，但捕食量並未改變，所以捕食風險的降低是由於獵物量增加所造成，但不可食獵物的死亡率會隨攻擊次數而逐漸降低(代表捕食者具有將色彩及味道進行關聯的學習能力)，因此作者認為在自然界中當不可食獵物增加時，並不會分散捕食風險，而是因為總族群量增加使個體被捕食風險降低。

兩種具共擬態關係毒蛺蝶視色素基因作用路徑之趨同與趨異表現

文獻來源: Ferguson LC, Jiggins CD. 2009. Shared and divergent expression domains on mimetic Heliconius wings. Evolution & Development 11(5): 498-512. [摘要網址]

簡介
毒蝶屬(Heliconius)為擬態生物學中穆氏擬態最具代表性的例子，自1879年穆氏擬態發表後，即吸引生物學家從多許多生物議題探討此龐大擬態群的產生，如行為學、演化學、化學生物學、群聚生態學，至近代的分子生物學、發育生物學等，但該擬態群的演化歷程仍然有許多的疑問未解。本篇文章從發育生物學的角度出發，嘗試以兩種毒蝶屬的物種，H. erato與H. melpomene，探索其相似翅紋的發育來源。作者觀察蛹發育時期時有關翅紋色素的基因發育表現，發現在兩個物種中，有關所有有關朱紅色色素形成的基因皆有關連，但其表現的形式有顯著的差異。兩個未在H. erato中研究的基因，scarlet與kf，增強H. melpomene的猩紅色素在翅紋中的呈現，可能暗示此兩種基因也在擬態的其他成員中參與翅紋的調控。

Abstract
Heliconius butterfly wing patterns show repeated convergence between species and have adaptive value in mimicry and mate choice, offering an opportunity to connect adaptive changes in phenotype with their underlying genotypes. Here we study forewing ommochrome pigmentation in Heliconius melpomene. We clone two new ommochrome pathway genes for the Lepidoptera, karmoisin and kynurenine formamidase (kf ), and analyze the expression patterns of all known ommochrome genes across pupal wing development. In combination with published work, this generates the first comparative gene expression data for the co-mimics Heliconius erato and H. melpomene. In both species cinnabar expression correlates with the forewing band, but the expression pattern of vermillion differs significantly between the mimics. This demonstrates that both shared and divergent expression patterns are associated with mimetic phenotypes between Heliconius species. Two genes not studied in H. erato, scarlet and possibly kf, also show enhanced expression in the forewing band of H. melpomene, implying co-ordinated upregulation of several members of this biosynthetic pathway during pattern formation.

Butterfly effects in mimicry? Combining signal and taste can twist the relationship of Müllerian co-mimics

Butterfly effects in mimicry? Combining signal and taste can twist the relationship of Müllerian co-mimics

Behavioural Evology and Sociobiology, Vol. 62, No. 8, 1267-1276

Eira Ihalainen, Leena Lindström, Johanna Mappes and Sari Puolakkainen
Department of Biological and Environmental Science, FI-40014 University of Jyväskylä

Müllerian co-mimics are aposematic species that resemble each other; sharing a warning signal is thought to be mutually beneficial for the co-mimics by reducing per capita predation risk. In Batesian mimicry, edible mimics avoid predation by resembling an aposematic model species. The protection of both the model and the mimic is weakened when the mimics are abundant compared to the models. The quasi-Batesian view suggests that defended (Müllerian) co-mimics, when unequal in their defences, could also show a Batesian-like trend of increasing mortality with increasing abundance of a less defended “mimic”. We manipulated frequencies of unequally distasteful artificial co-mimics that were prey for great tits. The co-mimics had different signals (imperfect mimicry) but were equally preferred by the birds when palatable. Unexpectedly, when unpalatable, one of the signals was easier for the birds to learn to avoid. Consequently, during predator learning, the signal design of the prey strongly affected mortality of the co-mimics; there was an interaction between the signal and frequency treatments, but increasing the frequency of a less defended “mimic” did not increase co-mimic mortalities as predicted. In contrast, in a memory test that followed, the effect of signal design disappeared; if the birds had experienced high frequency of “mimics” during learning, co-mimic mortalities did subsequently increase. Since the effect of co-mimic frequencies on mortalities changed depending on the signal design of the prey and predator experience, the results suggest that mimetic relationship may be an unpredictable interplay of several factors in addition to taste and abundance.

Keywords: Aposematism - Quasi-Batesian mimicry - Predator psychology - Avoidance learning - Memory

Identity of Euploea orontobates Fruhstorfer, 1910 (Lepidoptera: Nymphalidae), a milkweed butterfly from Thailand and Vietnam

Identity of Euploea orontobates Fruhstorfer, 1910 (Lepidoptera: Nymphalidae), a milkweed butterfly from Thailand and Vietnam

Zootaxa (2009) Vol. 1991, 43-50
A.L. MONASTYRSKII(1) & R.I. VANE-WRIGHT(2) 1Vietnam-Russia Research Tropical Centre 2Department of Entomology, the Natural History Museum, Cromwell Road, London SW7 5BD, UK; & Durrell Institute of Conservation and Ecology, University of Kent

Euploea orontobates Fruhstorfer, 1910, described from south-eastern Thailand (Si Racha district), is demonstrated to be a senior synonym of Euploea conbuom Saito & Inayoshi, 2006, from southern Central Vietnam. The relationships and biogeography of this rare butterfly are discussed, and presented together with comments on the principal mimicry complex among the Euploea species of Indochina.

Keywords: Danainae, Euploea orontobates, Euploea conbuom, synonymy, relationships, Thailand, Vietnam, Sundaland, endemism, biogeography

[Article]Learning and the mimicry spectrum: from quasi-Bates to super-Müller

Learning and the mimicry spectrum: from quasi-Bates to super-Müller

Alexandra C.V. Balogh^{, a,} , Gabriella Gamberale-Stille^a and Olof Leimar^a

^aDepartment of Zoology, Stockholm University, Sweden

Müllerian mimicry is the mutualistic resemblance between two defended species, while Batesian mimicry is the parasitic resemblance between a palatable species (the mimic) and an unpalatable one (the model). These two kinds of mimicry are traditionally seen as extreme ends of a mimicry spectrum. For the range in between, it has been suggested that mimetic relations between unequally defended species could be parasitic, and this phenomenon has been referred to as quasi-Batesian mimicry. Where a mimetic relation is placed along the mimicry spectrum depends on the assumptions made about predator learning. We used a variant of the Rescorla–Wagner learning model for virtual predators to analyse the different possible components of the mimicry spectrum. Our model entails that the rate of associative learning is influenced by variation in the stimuli to be learned. Variable stimuli, that is, unequal defences, can increase the predator learning rate and thus lead to an increased level of mutualism in a mimetic relation. In our analysis, we made use of the concepts of super-Müllerian mimicry, where the benefit of mimicry is even greater than in traditional Müllerian mimicry, and quasi-Müllerian mimicry, where mimicry by a palatable mimic is mutualistic. We suggest that these types of mimicry should be included in the mimicry spectrum along with Müllerian, Batesian and quasi-Batesian mimicry.

Keywords: associative learning; mutualism; Müllerian mimicry; quasi-Batesian mimicry; Rescorla–Wagner model

[Debate]珊瑚蛇與奶蛇擬態經典案例的諸多疑點

Milk snake與Coral snake所形成的putative mimicry complex成為擬態生物學研究的經典已達一世紀之久. 但是這個擬態群一直存在著兩個違背Batesian mimicry預測的基本問題: (1) 被認為是mimic的奶蛇數量遠比被認為是model的coral snake為多; (2) 兩者不一定(而且經常)是不共棲的. 針對model與mimic不一定共棲的問題, 已經有"allopatric mimicry"這個理論所討論, 對於兩者個相對豐度的問題則應追溯至Brower & Brower (1962)以及Greene & McDiarmid (1981)的文章. Harper & Pfennig (2008)的文章則以族群遺傳學的方法證實了身為mimic的milk snake雄性會進行遷徙, 而且遷徙到coral snake不存在的地區, 間接地提供allopatric mimicry存在的族群遺傳學事證. 然而倒底是什麼記憶力, 學習能力與辯識力好的predator讓allopatric mimicry能夠存在, 則應該是下一個研究的目標.

• Brattstrom, B.H. 1955. The Coral Snake 'Mimic' Problem and Protective Coloration. Evolution 9(2): 217-219.
• Dunn, E.R. 1949. Relative Abundance of Some Panamanian Snakes. Ecology 30(1): 39-57.
• Brower, L. P. & Brower, J. V. Z. 1962. The relative abundance of model and mimic butterflies in natural populations of the Battus philenor mimicry complex. Ecology 43: 154–158.
• Clarke, C. & Sheppard, P. M. 1975. The genetics of the mimetic butterfly Hypolimnas bolina (L.). Phil. Trans. R. Soc. B 272: 229–265.
• Greene, H. W. & McDiarmid, R. Y. 1981. Coral snake mimicry: does it occur? Science 213: 1207–1212.
• Harper, G.R., Pfennig, D.W. 2008. Selection overrides gene flow to break down maladaptive mimicry. Nature 451: 1103-1106.
• Pfennig, D. W., Harcombe, W. R. & Pfennig, K. S. 2001. Frequency-dependent Batesian mimicry. Nature 410: 323.
• Ruxton, G. D., Sherratt, T. N. & Speed, M. P. 2004. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford Univ. Press, Oxford.
• Waldbauer, G. P. & Sternburg, J. G. 1987. Experimental field demonstration that two aposematic butterfly color patterns do not confer protection against birds in Northern Michigan. Am. Midl. Nat. 118: 145–152.
• Wallace, A. R. 1870. Contributions to the Theory of Natural Selection, Macmillan, London.

其它以奶蛇/珊瑚蛇所形成的擬態群為研究的文章可見David W. Pfennig研究群的著作目錄.

[Article]Conflict btw natural & sexual selection due to mmicry

Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species?

Journal of Evolutionary Biology

Volume 21 Issue 3 Page 749-760, May 2008

Citation: C. ESTRADA, C. D. JIGGINS (2008) Interspecific sexual attraction because of convergence in warning colouration: is there a conflict between natural and sexual selection in mimetic species? Journal of Evolutionary Biology 21 (3) , 749–760 doi:10.1111/j.1420-9101.2008.01517.x

Abstract

When species converge in their colour patterns because of mimicry, and those patterns are also used in mate recognition, there is a probability of conflicting selection pressures. Closely related species that mimic one another are particularly likely to face such confusion because of similarities in their courtship behaviour and ecology. We conducted experiments in greenhouse conditions to study interspecific attraction between two mimetic butterfly species, Heliconius erato and Heliconius melpomene. Both species spent considerable time approaching and courting females of the co-mimic species. Experiments using wing models demonstrated the importance of colour pattern in this interspecific attraction. Although males of H. melpomene were attracted to their co-mimics as much as to their own females, H. erato males were more efficient at distinguishing conspecifics, possibly using wing odours. Although preliminary, these results suggest that the use of additional cues may have evolved in H. erato to reduce the cost of convergence in visual signals with H. melpomene. Overall, our results showed that there might be a cost of mimetic convergence because of a reduction in the efficiency of species recognition. Such cost may contribute to explain the apparently stable diversity in Müllerian mimetic patterns in many tropical butterfly assemblages.

[Article]Can experienced birds select for Müllerian mimicry?

link: http://tinyurl.com/2m6zlz
Ihalainen, E. et al. 2008. Behav. Ecol. 19: 362-368
Abstract: Field experiments have shown that avian predators in the wild can select for similarity of warning signals in aposematic prey (Müllerian mimicry) because a common signal is better protected than a signal that is novel and rare. The original theory of Müllerian mimicry assumes that the mechanism promoting mimicry is predator learning; by sharing a signal, the comimic species share the mortality that is due to sampling by inexperienced predators. Predation events have not been observed in the wild, and learning experiments with naive bird predators in a laboratory have not unambiguously shown a benefit of a uniform signal compared with different signals. As predators in the field experiments are likely to be more experienced compared with previous laboratory experiments, we studied selection by experienced predators on a novel imperfect mimic. We trained great tits Parus major to avoid artificial aposematic models and subsequently introduced perfect and imperfect mimics at different frequencies. Birds with prior experience on the models selected against the imperfect mimics that were at a disadvantage also in a memory test conducted a week after their introduction. Selection against the imperfect mimics was antiapostatic. However, the imperfect mimics also benefited from some signal generalization to the models and possibly gained protection because the birds were familiar with the alternative cryptic prey that was also present. Our results suggest that experienced predators might be more important to the evolution of mimicry than the learning-based theory assumes.

[Article]A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies

Link: http://0rz.tw/733NG
Abstract: We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Müllerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius melpomene, maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a “supergene”, determining multiple sympatric morphs in a third species, H. numata. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic “supergene” polymorphism without intermediates. Although we cannot at this stage confirm the homology of the loci segregating in the three species, our results imply that a conserved yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions.