Mullerian Mimicry: Sharing the Load Reduces the Legwork

Color pattern mimicry has long been held up as a powerful example of natural selection. A recent study supports the theory by describing Mu¨ llerian mimicry rings in Appalachian millipedes that are analogous to those observed in tropical butterflies.

Dispatch R687 Yokoyama, K., Oksche, A., Darden, T.R., and Farner, D.S (1978) The sites of encephalic photoreception in the photoperiodic induction of growth of the testes in the white crowned sparrow, Zonotrichia leucophrys gambelii Cell Tiss Res 189, 441–467 Nakao, N., Ono, H., Yamamura, T., Anraku, T., Takagi, T., Higashi, K., Yasuo, S., Katou, Y., Kageyama, S., Uno, Y., et al (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response Nature 452, 317–322 Halford, S., Pires, S.S., Turton, M., Zheng, L., Gonzalez-Menendez, I., Peirson, S.N., Jose, M., Garcia-Fernandez, J.M., Hankins, M.W., and Foster, R.G (2009) VA-opsin-based photoreceptors in the hypothalamus of birds Curr Biol 19, 1396–1402 Foster, R.G., Follett, B.K., and Lythgoe, J.N (1985) Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail Nature 313, 50–52 Hanon, E.A., Lincoln, G.A., Fustin, J.M., Dardente, H., Masson-Pe´vet, M., Morgan, P.J., and Hazlerigg, D.G (2008) Ancestral TSH mechanism signals summer in a photoperiodic mammal Curr Biol 18, 1147–1152 Rodriguez, E.M., Blazquez, J.L., Pastor, F.E., Pelaez, B., Pena, P., Peruzzo, B., and Amat, P (2005) Hypothalamic tanycytes: a key 10 11 12 13 14 15 16 component of brain-endocrine interaction Int Rev Cytol 247, 89–164 Goldman, B.D (2001) Mammalian photoperiodic system: formal properties and neuroendocrine mechanisms of photoperiodic time measurement J Biol Rhythms 16, 283–301 Morgan, P.J., Barrett, P., Howell, H.E., and Helliwell, R (1994) Melatonin receptors: localization, molecular pharmacology and physiological significance Neurochem Int 24, 101–146 Lincoln, G.A., Andersson, H., and Loudon, A (2003) Clock genes in calendar cells as the basis of annual timekeeping in mammals–a unifying hypothesis J Endocrinol 1179, 1–13 Menaker, M (1968) Extraretinal light perception in the sparrow I Entrainment of the biological clock Proc Natl Acad Sci USA 59, 414–421 Sharp, P.J (2005) Photoperiodic regulation of seasonal breeding in birds Ann N.Y Acad Sci 1040, 189–199 Reppert, S.M., Weaver, D.R., Cassone, V.M., Godson, C., and Kolakowski, L.F (1995) Melatonin receptors are for the birds molecular analysis of receptor subtypes differentially expressed in chick brain Neuron 15, 1003–1015 Dufourny, L., Levasseur, A., Migaud, M., Isabelle Callebaut, I., Pontarotti, P., Malpaux, B., and Mu¨llerian Mimicry: Sharing the Load Reduces the Legwork Color pattern mimicry has long been held up as a powerful example of natural selection A recent study supports the theory by describing Mu¨llerian mimicry rings in Appalachian millipedes that are analogous to those observed in tropical butterflies Richard M Merrill and Chris D Jiggins ‘‘‘Natural Selection’ explains almost everything in Nature’’, Wallace wrote to Darwin, just a year after the publication of the Origin, ‘‘but there is one class of phenomena I cannot bring under it — the repetition of the forms and colours of animals in distinct groups, but the two always occurring in the same country and generally on the very same spot’’ [1] Wallace need not have worried as mimicry soon became, and remains, one of the most intriguing and powerful examples of natural selection This has once again been demonstrated by a new study of Appalachian millipedes [2] In 1862, Henry Walter Bates [3] suggested that perfectly tasty individuals might gain an advantage by mimicking unpalatable or dangerous species, effectively parasitizing the warning signal of the model A few years later, Johannes Friedrich (‘Fritz’) Mu¨ller, a German emigrant to Brazil, proposed an alternative but related hypothesis, whereby unpalatable species benefit by converging on the same warning pattern, thereby more efficiently advertising their distastefulness to potential predators [4] Mu¨ller’s description of mutualistic mimicry included what was perhaps the first mathematical model in evolutionary biology [5] Bates and Mu¨ller were both heavily influenced by their travels in South America In particular, widespread mimicry between unpalatable tropical butterflies struck a chord with Mu¨ller As recently demonstrated by Marek and Bond [2], however, Mu¨llerian mimicry is neither an exclusively tropical nor an exclusively lepidopteron phenomenon In their study, seven species of brightly colored Apheloriine millipedes, all endemic to the temperate forests of the Appalachian Mountains in the United States, are shown to form Mu¨llerian mimicry Monget, P (2008) GPR50 is the mammalian ortholog of Mel1c: Evidence of rapid evolution in mammals BMC Evol Biol 8, 105 17 Ivanova, E.A., Bechtold, D.A., Dupre, S.M., Brennand, J., Barrett, P., Luckman, S.M., and Loudon, A.S.I (2008) Altered metabolism in the melatonin-related receptor (GPR50) knockout mouse Am J Physiol 294, E176–E182 18 Warren, W.C., Hillier, L.W., Marshall Graves, J.A., Birney, E., Ponting, C.P., Grutzner, F., Belov, K., Miller, W., Clarke, L., Chinwalla, A.T., et al (2008) Genome analysis of the platypus reveals unique signatures of evolution Nature 453, 175–183 19 Davies, W.L., Carvalho, L.S., Cowing, J.A., Beazley, L.D., Hunt, D.M., and Arrese, C.A (2007) Visual pigments of the platypus: A novel route to mammalian colour vision Curr Biol 17, R161–R163 School of Biological Sciences, Zoology Building, University of Aberdeen Tillydrone Avenue, Aberdeen AB23 2TZ, Scotland *E-mail: d.hazlerigg@abdn.ac.uk DOI: 10.1016/j.cub.2009.07.036 rings, or groups of species sharing a mimetic pattern, analogous to those of tropical butterflies (Figure 1) Interestingly, apheloriines lack eyes, making them a particularly good system in which to study warning mimicry — being blind there can be no sexual selection acting on warning color In contrast, many other mimetic species, such as Heliconius butterflies, use color patterns in mate choice, such that multiple selection pressures need to be considered to fully understand color pattern evolution [6] To human observers, co-occurring millipede species look strikingly similar In order to quantify this similarity, Marek and Bond [2] measured spectral reflectance of coloured spots and corrected for the forest light environment They then applied an arbitrary similarity threshold to classify species as mimetic within a site Their use of spectral reflectance measurements clearly improves on a purely subjective assessment of mimicry by human observers, but the degree of similarity required to classify two taxa as mimetic remains arbitrary As has been recognised for some time, a better knowledge of the discriminatory powers of relevant predators would greatly enhance our understanding of mimicry and of the degree of similarity necessary to generate a selective advantage [7] Current Biology Vol 19 No 16 R688 Figure Mu¨llerian mimicry in North American Apheloriine millipedes, Neotropical Heliconius butterflies and Peruvian Ranitomeya (Dendrobates) frogs In each case, populations of distantly related species converge on the same brightly colored warning pattern within a single locality, but show geographically concordant diversity across their range (A) Millipedes of the Apheloria clade (top row) and their mimics in the Brachoria clade (bottom row) (B) Heliconius erato (top row) and its mimic Heliconius melpomene (bottom row) (C) Ranitomeya imitator (left in both panels) and its mimics R surmmersi (left panel) and R ventrimaculata (right panel) Photo credits: (A) Paul Marek; (B) Bernard D’Abrera; (C) Jason Brown A phylogeny of the millipedes was then used to demonstrate that pattern similarity was not solely due to common ancestry Indeed, similar patterns were repeatedly observed in divergent clades, providing convincing evidence for convergent evolution The pattern is reminiscent of that seen in neotropical Heliconius butterflies, where pairs of mimetic species are found in the two most divergent clades of the genus [8] Mu¨llerian mimicry theory predicts that less abundant species will evolve to mimic a more abundant or better-defended ‘model’ This has been termed ‘advergence’, to contrast with the alternative of ‘convergence’, where both species evolve towards an intermediate pattern Among the millipedes, estimates of current abundance based on field capture data, and of historical population size derived from genetic data, both indicate that the Apeloria clade are more common than the Brachoria clade Thus, it seems most likely that the former represent the ‘models’ and the latter ‘mimics’ Nonetheless, while we agree that this is certainly the most probable scenario, the data certainly not convincingly rule out alternatives Neutral molecular markers may indicate that Apeloria clade species are older, but this does not rule out more recent and ongoing colour pattern evolution, perhaps involving coevolution with Brachoria As in other mimicry systems, a definitive answer regarding the evolutionary history of the patterns will require sequencing the genes that actually control color patterns, rather than making inferences from unlinked neutral markers Apheloriine millipedes are therefore comparable to better-known, tropical examples of Mu¨llerian mimicry such as Dendrobates frogs [9] and the diverse mimicry complexes involving neotropical heliconiine and ithomiine butterflies [8,10] In particular, the two Heliconius species H erato and H melpomene converge on the same brightly colored warning pattern within a single locality but show striking, geographically concordant diversity across their range, much like the Apheloriine millipedes Similarly H erato, like the Apheloria clade millipedes, is often more locally abundant and frequently considered the ‘model’ [11] Apart from being a compelling new example, the Appalachian millipedes tell us anything new about Mu¨llerian mimicry generally? There seem to be interesting differences between temperate and tropical systems Mu¨llerian mimicry in temperate areas is often ‘impressionistic’, a good example being bumble bees, which show geographically convergent patterns but not precise mimicry [7] The Appalachian millipedes similarly show varying degrees of perfection in their mimetic patterns and are described as ‘impressionistic’ This contrasts with the repeated, astonishingly precise mimicry among Heliconius butterflies One reason for this difference may be that temperate Mu¨llerian mimics tend to be dangerous rather than simply unpalatable Remarkably, Marek and Bond [2] note that a single millipede ‘‘can secrete 18fold the amount of hydrogen cyanide Dispatch R689 necessary to kill a pigeon-sized bird’’, whereas mimetic tropical butterflies are often merely described as ‘distasteful’ Truly nasty Mu¨llerian mimics are found in the tropics — poison arrow frogs are clearly a little more than ‘distasteful’ [9] and pitvipers are, after all, best avoided [12] — but perhaps nearer the equator mimicry can also evolve more easily among less well defended species The diversity of predators is much greater in the tropics, and there are more insectivores specialising on flying insects such as butterflies, so mimicry may be favored for signalling to particular predators The great diversity of potential prey may also increase the selection pressure for mimicry, as predators are unlikely to be capable of learning a vast diversity of suitable prey in tropical communities [5] Additionally, birds, often implicated as the ‘predator’ in mimicry systems, are known to live longer in the tropics, offering greater opportunity for learning [13] A recent review of warning coloration and mimicry recommends that ‘‘more experimental field studies, especially with non-lepidopteran groups’’ are needed to better understand the phenomenon [7] The Appalachian millipedes offer a great opportunity to study poorly understood aspects of Mu¨llerian mimicry, such as predator discrimination and perception, the strength of selection for mimicry and the reasons for geographical heterogeneity in mimicry signals Overall, however, this is an elegant new example of Mu¨llerian mimicry, an evolutionary phenomenon that remains one of the most compelling examples of natural selection, 130 years after its first discovery References Wallace, A.R (1860) Letter 2627—Wallace, A.R to Darwin, C.R (http://www.darwinproject ac.uk/darwinletters/calendar/entry-2627.html, University of Cambridge) Marek, P.E., and Bond, J.E (2009) A Mu¨llerian mimicry ring in Appalachian millipedes Proc Natl Acad Sci USA 106, 9755–9760 Bates, H.W (1862) Contributions to an insect fauna of the Amazon valley (Lepidoptera: Heliconidae) Trans Linn Soc Lond 23, 495–566 Mu¨ller, F (1879) Ituna and Thyridia; a remarkable case of mimicry in butterflies Trans Entomol Soc Lond 1879, xx–xxix Sherrat, T.N (2008) The evolution of Mu¨llerian mimicry Naturwissenschaften 95, 681–695 Jiggins, C.D., Naisbit, R.E., Coe, R.L., and Mallet, J (2001) Reproductive isolation Microbial Interactions: Bacteria Talk to (Some of) Their Neighbors A recent study reports that Bacillus subtilis biofilm formation depends upon paracrine signaling where the signal-producing and target-responsive cells are different Ishita M Shah and Jonathan Dworkin Bacteria rely on precisely coordinated signaling mechanisms to ensure efficient and accurate transmission of chemical messages within a population During bacterial differentiation, this signaling has been thought to be autocrine — that is, all cells produce and respond to the same signal However, in a recent paper in Genes and Development, Lopez et al [1] report that biofilm formation in Bacillus subtilis involves paracrine signaling Specifically, they found that, while most cells within the population produce a prenylated peptide, this molecule triggers the production of another signaling molecule — surfactin — only in a small subset of cells As a consequence, a subpopulation of cells not capable of producing surfactin responds to surfactin to produce the extracellular matrix component of the biofilm In autocrine signaling the same cells both produce and respond to a signal, whereas in paracrine signaling the producing and receiving cells are different While paracrine signaling controls eukaryotic processes dependent on cell–cell signaling, such as neurotransmission, blood clotting, angiogenesis, and embryonic differentiation, cell–cell communication in bacteria has been thought to be autocrine For example, the phenomenon of quorum sensing 10 11 12 13 caused by colour pattern mimicry Nature 411, 302–305 Ruxton, G.D., Sherrat, T.N., and Speed, M.P (2004) Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry (Oxford, UK: Oxford University Press) Beltra´n, M., Jiggins, C.D., Brower, A.V.Z., Bermingham, E., and Mallet, J (2007) Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from a multilocus DNA sequence data Biol J Linn Soc 92, 221–239 Symula, R., Schulte, R., and Summers, K (2001) Molecular phylogenetic evidence for a mimetic radiation in Peruvian poison frogs supports a Mullerian mimicry hypothesis Proc R Soc Lond B 268, 2415–2421 Jiggins, C.D., Mallarino, R., Willmott, K.R., and Bermingham, E (2006) The phylogenetic pattern of speciation and wing pattern change in neotropical Ithomia butterflies (Lepidoptera: Nymphalidae) Evolution 60, 1454–1466 Mallet, J (1999) Causes and consequences of a lack of coevolution in Mu¨llerian mimicry Evol Ecol 13, 777–806 Sanders, K.L., Malhotra, A., and Thorpe, R.S (2006) Evidence for A Mu¨llerian mimetic radiation in Asian pitvipers Proc R Soc Lond B 273, 1135–1141 Stutchbury, B.J.M., and Morton, E.S (2000) Behavioral Ecology of Tropical Birds (London: Academic Press) Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK E-mail: c.jiggins@zoo.cam.ac.uk DOI: 10.1016/j.cub.2009.07.008 involves the detection of a threshold concentration of a signaling molecule by bacteria that also produce these signals (Figure 1A) [2] In the case of quorum sensing in Vibrio species, AHL autoinducers are detected by cytoplasmic proteins like LuxR, which activate transcription of quorum-sensing genes upon binding to their partner autoinducers [3] Similarly, the B subtilis genetic competence regulator ComX is recognized by a sensor histidine kinase that triggers phosphorylation events necessary for proper target gene expression [4] While these responses can occur over distances within bacterial populations, signaling that requires cells to be in close proximity to one another can also occur For example, during fruiting body formation in Myxococcus xanthus, a signal protein is displayed on the surface and interacts with a receptor on an adjacent cell to transmit signal Both cells express the signaling molecule as well as the receptor (Figure 1B) [5] Another