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overcome the chemical defenses of the toxic frogs after their death. The results of the study showed that the snake became accustomed to the differences in the frogs by their hold and release timing, always holding the nontoxic, while always releasing the highly toxic frogs, with the frogs that discharge mucus somewhere in between. The snakes would also spend generously more time gaped between the release of the highly toxic frogs than the short gaped time between the release of the frogs that discharge mucus. Therefore, the snakes have a much higher advantage of being able to cope with the different frogs defensive mechanisms, while the frogs could eventually increase the potency of their toxic knowing the snakes would adapt to that change as well, such as the snakes having venom themselves for the initial attack. The coevolution is still highly asymmetrical because of the advantage the predators have over their prey.
127:. This antagonistic relationship leads to the necessity for the pathogen to have the best virulent alleles to infect the organism and for the host to have the best resistant alleles to survive parasitism. As a consequence, allele frequencies vary through time depending on the size of virulent and resistant populations (fluctuation of genetic selection pressure) and generation time (mutation rate) where some genotypes are preferentially selected thanks to the individual fitness gain. Genetic change accumulation in both populations explains a constant adaptation to have lower fitness costs and avoid extinction in accordance with the
294:
demonstrate an ability to resist low levels of the toxin, suggesting an ancestral predisposition to tetrodotoxin resistance. The lower levels of resistance in separated populations suggest a fitness cost of both toxin production and resistance. Snakes with high levels of tetrodotoxin resistance crawl more slowly than isolated populations of snakes, making them more vulnerable to predation. The same pattern is seen in isolated populations of newts, which have less toxin in their skin. There are geographic hotspots where levels of tetrodotoxin and resistance are extremely high, showing a close interaction between newts and snakes.
903:
153:
180:(mobile spores, characteristics of oomycetes) are liberated by zoosporangia provided from a mycelium and brought by rain or wind before infecting tubers and leaves. Black colours appear on the plant because of the infection of its cellular system necessary for the multiplication of the oomycete infectious population. The parasite contains virulent-avirulent allelic combinations in several microsatellite loci, likewise the host contains several multiloci resistance genes (or
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249:
the ultrasound by slowing their flight times, while only one of the endemic species reacted to the ultrasound signal, indicating a loss of hearing over time in the endemic population. However, the degree of loss or regression depends on the amount of evolutionary time and whether or not the moth species has developed secondary uses for hearing.
258:
than other, louder bat species. Moths have further evolved the ability to discriminate between high and low echolocation click rates, which indicates whether the bat has just detected their presence or is actively pursuing them. This allows them to decide whether or not defensive ultrasonic clicks are worth the time and energy expenditure.
290:
resistance creates a selective pressure that favors newts that produce more toxin. That in its turn imposes a selective pressure favoring snakes with mutations conferring even greater resistance. This evolutionary arms race has resulted in the newts producing levels of toxin far in excess of that needed to kill any other predator.
257:
bats have evolved to use a quieter mode of echolocation, calling at a reduced volume and further reducing the volume of their clicks as they close in on prey moths. The lower volume of clicks reduces the effective successful hunting range, but results in a significantly higher number of moths caught
248:
studies. In places with spatial or temporal isolation between bats and their prey, the moth species hearing mechanism tends to regress. Fullard et al. (2004) compared adventive and endemic
Noctiid moth species in a bat-free habitat to ultrasound and found that all of the adventive species reacted to
289:
is resistant to the toxin. While in principle the toxin binds to a tube-shaped protein that acts as a sodium channel in the snake's nerve cells, a mutation in several snake populations configures the protein in such a way as to hamper or prevent binding of the toxin, conferring resistance. In turn,
315:
Floodplain death adders eat three types of frogs: one nontoxic, one producing mucus when taken by the predator, and the highly toxic frogs, however, the snakes have also found if they wait to consume their toxic prey the potency decreases. In this specific case, the asymmetry enabled the snakes to
306:
predators used their own shell to open the shell of their prey, oftentimes breaking both shells of the predator and prey in the process. This led to the fitness of larger-shelled prey to be higher and then more selected for through generations, however, the predator's population selected for those
336:
well before it could ever hope to adapt to a new predator, competitor, etc. This should not seem surprising, as one species may have been in evolutionary struggles for millions of years while the other might never have faced such pressures. This is a common problem in isolated ecosystems such as
293:
In populations where garter snakes and newts live together, higher levels of tetrodotoxin and resistance to it are observed in the two species respectively. Where the species are separated, the toxin levels and resistance are lower. While isolated garter snakes have lower resistance, they still
252:
Some bats are known to use clicks at frequencies above or below moths' hearing ranges. This is known as the allotonic frequency hypothesis. It argues that the auditory systems in moths have driven their bat predators to use higher or lower frequency echolocation to circumvent the moth hearing.
240:
subfamily of
Noctuid moths uniquely respond to bat echolocation in three prevailing hypotheses: startle, sonar jamming, and acoustic aposematic defense. All these differences depend on specific environmental settings and the type of echolocation call; however, these hypotheses are not mutually
114:
Arms races may be classified as either symmetrical or asymmetrical. In a symmetrical arms race, selection pressure acts on participants in the same direction. An example of this is trees growing taller as a result of competition for light, where the selective advantage for either species is
210:
bat vocalizations during prey approach. The recording covers a total of 1.1 seconds; lower main frequency ca. 45 kHz (as typical for a common pipistrelle). About 150 milliseconds before final contact time between and duration of calls are becoming much shorter
1163:
Brodie, Edmund D.; Feldman, Chris R.; Hanifin, Charles T.; Motychak, Jeffrey E.; Mulcahy, Daniel G.; Williams, Becky L.; Brodie, Edmund D. Jr. (2005). "Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution".
115:
increased height. An asymmetrical arms race involves contrasting selection pressures, such as the case of cheetahs and gazelles, where cheetahs evolve to be better at hunting and killing while gazelles evolve not to hunt and kill, but rather to evade capture.
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who were more efficient at opening the larger-shelled prey. This example is an excellent example of asymmetrical arms race because while the prey is evolving a physical trait, the predators are adapting in a much different way.
221:
1080:
Brodie, E.; Brodie, E. D.; Ridenhour, B. (2003). "The evolutionary response of predators to dangerous prey: Hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts".
188:
and is, in general, widespread in plant diseases. Expression of genetic patterns in the two species is a combination of resistance and virulence characteristics in order to have the best survival rate.
1215:
Brodie, Edmund D.; Brodie, Edmund D. Jr (1991). "Evolutionary response of predators to dangerous prey: Reduction of toxicity of newts and resistance of garter snakes in island populations".
236:
have in turn evolved to detect the echolocation calls of hunting bats, and evoke evasive flight maneuvers, or reply with their own ultrasonic clicks to confuse the bat's echolocation. The
727:
Muma, K. E.; Fullard, J. H. (2004). "Persistence and regression of hearing in the exclusively diurnal moths, Trichodezia albovittata (Geometridae) and
Lycomorpha pholus (Arctiidae)".
220:
74:. Alternatively, the arms race may be between members of the same species, as in the manipulation/sales resistance model of communication (Dawkins & Krebs, 1979) or as in
469:
da Cruz, João Filipe; Gaspar, Helena; Calado, Gonçalo (29 November 2011). "Turning the game around: toxicity in a nudibranch-sponge predator–prey association".
172:
potato varieties. It was created in the
Netherlands in the early 20th century and now is mainly cultivated in the North of France and Belgium. The oomycete
1296:
Phillips, Ben; Shine, Richard (December 2007). "When Dinner Is
Dangerous: Toxic Frogs Elicit Species-Specific Responses from a Generalist Snake Predator".
222:
439:
New York: W. W. Norton. Note: This book was also published by
Penguin in 1991. While the text is identical, page numbers differ
521:"Differential interaction of Phytophthora infestans on tubers of potato cultivars with different levels of blight resistance"
456:
1360:
Conner, W. E.; Corcoran, A. J. (2012). "Sound strategies: the 65-million-year-old battle between bats and insects".
1028:"Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey"
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633:
918:"The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly pre"
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405:
332:
When a species has not been subject to an arms race previously, it may be at a severe disadvantage and face
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Goerlitz, Holger R.; ter
Hofstede, Hannah M.; Zeale, Matt R. K.; Jones, Gareth; Holderied, Marc W. (2010).
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Evolutionarily speaking, insects have responded to selective pressure from bats with new evasive mechanisms
614:"How Some Insects Detect and Avoid Being Eaten by Bats: Tactics and Countertactics of Prey and Predator"
328:
Cane Toads have experienced a massive population explosion in
Australia due to the lack of competition.
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The different defense mechanisms have been shown to be directly responsive to bat echolocation through
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613:
206:
128:
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79:
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58:. The co-evolving gene sets may be in different species, as in an evolutionary arms race between a
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Brodie, Edmund D.; Brodie, Edmund D. Jr.; Motychak, Jeffrey E. (2002). "Recovery of garter snakes (
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Flier, W. G.; Turkensteen, L. J.; van den Bosch, G. B. M.; Vereijken, P. F. G.; Mulder, A. (2001).
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977:"The Chemical and Evolutionary Ecology of Tetrodotoxin (TTX) Toxicity in Terrestrial Vertebrates"
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Competition of sets of genes, traits, or species, that develop adaptations against each other
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357:, have spread rapidly due to a lack of competition and a lack of adaptations to cane toad
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is responsible for the potato blight, in particular during the
European famine in 1840.
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and counter-adaptations against each other, resembling the geopolitical concept of an
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565:"Extinction of the acoustic startle response in moths endemic to a bat-free habitat"
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Ratcliffe, John M.; Fullard, James H.; Arthur, Benjamin J.; Hoy, Ronald R. (2010).
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862:"Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats"
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813:"An Aerial-Hawking Bat Uses Stealth Echolocation to Counter Moth Hearing"
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Yager, D. D. (2012). "Predator detection and evasion by flying insects".
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Feldman, C. R.; Brodie, E. D.; Brodie, E. D.; Pfrender, M. E. (2010).
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Feldman, C. R.; Brodie, E. D.; Brodie, E. D.; Pfrender, M. E. (2009).
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have evolved to use echolocation to detect and catch their prey.
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451:"La guerre des sexes chez les animaux" Eds Odile Jacob, Paris
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10.1554/0014-3820(2002)056[2067:teropt]2.0.co;2
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10.1641/0006-3568(2001)051[0570:HSIDAA]2.0.CO;2
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emphasized the role of such antagonistic interactions in
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Fullard, J. H.; Ratcliffe, J. M.; Soutar, A. R. (2004).
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exclusive and can be used by the same moth for defense.
82:
effects. One example of an evolutionary arms race is in
1032:
Proceedings of the Royal
Society B: Biological Sciences
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Proceedings of the Royal Society B: Biological Sciences
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have skin glands that contain a powerful nerve poison,
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1079:
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Floodplain death adders and separate species of frogs
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123:Selective pressure between two species can include
262:The rough-skinned newt and the common garter snake
612:Miller, Lee A.; Surlykke, Annemarie (July 2001).
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86:between the sexes, often described with the term
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1348:(1979). Arms races between and within species.
298:Predator whelk and the hard-shelled bivalve prey
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772:"Bats and moths: what is there left to learn?"
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1396:Nature's Eternal Arms Race (PBS Documentary)
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1128:) from the effects of tetrodotoxin. Hpet".
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285:. Throughout much of the newt's range, the
54:. These are often described as examples of
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110:Symmetrical versus asymmetrical arms races
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1258:Dietl, Gregory P. (3 November 2003).
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361:on the part of potential predators.
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1374:10.1146/annurev-ento-121510-133537
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662:"Bat and moth arms race revealed"
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1277:10.1046/j.1095-8312.2003.00255.x
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789:10.1111/j.1365-3032.2003.00355.x
749:10.1111/j.0307-6946.2004.00655.x
660:Palmer, Jason (19 August 2010).
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538:10.1046/j.1365-3059.2001.00574.x
506:(1973). A new evolutionary law,
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686:Current Opinion in Neurobiology
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46:traits that develop escalating
27:is an ongoing struggle between
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184:). That interaction is called
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975:Hanifin, Charles T. (2010).
365:are a major reason why some
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1166:Journal of Chemical Ecology
508:Evolutionary Theory 1, 1¬30
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377:, as was the case with the
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698:10.1016/j.conb.2011.12.011
217:Corresponding audio file:
186:gene-for-gene relationship
148:/Bintje potato interaction
1186:10.1007/s10886-005-1345-x
838:10.1016/j.cub.2010.07.046
483:10.1007/s00049-011-0097-z
406:Parent–offspring conflict
207:Pipistrellus pipistrellus
125:host-parasite coevolution
776:Physiological Entomology
416:Evolutionary anachronism
411:Antimicrobial resistance
391:Anti-predator adaptation
283:anti-predator adaptation
104:antagonistic coevolution
1298:The American Naturalist
943:10.1073/pnas.0901224106
100:character displacements
1130:Journal of Herpetology
1044:10.1098/rspb.2010.0748
878:10.1098/rspb.2010.1488
770:Waters, D. A. (2003).
345:. In Australia, many
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174:Phytophthora infestans
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146:Phytophthora infestans
129:Red Queen's hypothesis
66:(Vermeij, 1987), or a
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729:Ecological Entomology
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119:Host–parasite dynamic
1411:Evolutionary biology
436:The Blind Watchmaker
21:evolutionary biology
1178:2005JCEco..31..343B
1126:Thamnophis sirtalis
1038:(1698): 3317–3325.
934:2009PNAS..10613415F
928:(32): 13415–13420.
829:2010CBio...20.1568G
741:2004EcoEn..29..718M
287:common garter snake
275:Rough-skinned newts
433:Dawkins, R. 1996.
363:Introduced species
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320:Introduced species
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270:Rough-skinned newt
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994:10.3390/md8030577
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88:Fisherian runaway
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402:interactions
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255:Barbastelle
202:Spectrogram
98:leading to
48:adaptations
33:co-evolving
1405:Categories
621:BioScience
422:References
371:endangered
367:indigenous
359:bufotenine
351:cane toads
349:, such as
334:extinction
166:Munstersen
44:behavioral
40:phenotypic
1368:: 21–39.
1356::489-511.
1217:Evolution
1083:Evolution
547:0032-0862
339:Australia
238:Arctiidae
178:Zoospores
135:in 1973.
96:evolution
80:Red Queen
52:arms race
29:competing
1382:21888517
1318:18171175
1245:28564068
1202:16542226
1194:15856788
1103:12449493
1062:20522513
1013:20411116
962:19666534
896:20719772
847:20727755
798:86269745
757:83732973
714:24365000
706:22226428
667:BBC News
591:15271085
491:17819241
396:Parasite
385:See also
373:or even
281:, as an
246:sympatry
139:Examples
70:and its
68:parasite
60:predator
31:sets of
1336:General
1326:9744969
1237:2409496
1174:Bibcode
1150:1565808
1111:8251443
1053:2981930
1004:2857372
953:2726340
930:Bibcode
887:3013417
825:Bibcode
737:Bibcode
599:1054325
375:extinct
355:rabbits
341:or the
170:Fransen
1416:Mating
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182:R gene
162:Bintje
1354:B 205
1322:S2CID
1233:JSTOR
1198:S2CID
1146:JSTOR
1107:S2CID
794:S2CID
753:S2CID
710:S2CID
617:(PDF)
595:S2CID
487:S2CID
304:whelk
234:Moths
36:genes
23:, an
1378:PMID
1314:PMID
1241:PMID
1190:PMID
1099:PMID
1058:PMID
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958:PMID
922:PNAS
892:PMID
843:PMID
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587:PMID
543:ISSN
453:ISBN
400:host
379:dodo
353:and
302:The
230:Bats
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168:and
160:The
144:The
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64:prey
42:and
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1138:doi
1091:doi
1048:PMC
1040:doi
1036:277
999:PMC
989:doi
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938:doi
926:106
882:PMC
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833:doi
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