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Evolutionary arms race

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In evolutionary biology, an evolutionary arms race is an ongoing struggle between competing sets of co-evolving genes, phenotypic and behavioral traits that develop escalating adaptations and counter-adaptations against each other, resembling the geopolitical concept of an arms race. These are often described as examples of positive feedback.[1] The co-evolving gene sets may be in different species, as in an evolutionary arms race between a predator species and its prey (Vermeij, 1987), or a parasite and its host. 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 runaway evolution or Red Queen effects. One example of an evolutionary arms race is in sexual conflict between the sexes, often described with the term Fisherian runaway. Thierry Lodé[2] emphasized the role of such antagonistic interactions in evolution leading to character displacements and antagonistic coevolution.

Symmetrical versus asymmetrical arms races

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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 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.[3]

Host–parasite dynamic

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Selective pressure between two species can include host-parasite coevolution. 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 Red Queen's hypothesis suggested by Leigh Van Valen in 1973.[4]

Examples

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The Phytophthora infestans/Bintje potato interaction

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Bintje potatoes

The Bintje potato is derived from a cross between Munstersen and Fransen 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 Phytophthora infestans is responsible for the potato blight, in particular during the European famine in 1840. Zoospores (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 R gene). That interaction is called gene-for-gene relationship 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.[5]

Bats and moths

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Spectrogram of Pipistrellus pipistrellus 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 ("feeding buzz").
Corresponding audio file:

Bats have evolved to use echolocation to detect and catch their prey. Moths have in turn evolved to detect the echolocation calls of hunting bats, and evoke evasive flight maneuvers,[6][7] or reply with their own ultrasonic clicks to confuse the bat's echolocation.[8] The Arctiidae subfamily of Noctuid moths uniquely respond to bat echolocation in three prevailing hypotheses: startle, sonar jamming, and acoustic aposematic defense.[9] All these differences depend on specific environmental settings and the type of echolocation call; however, these hypotheses are not mutually exclusive and can be used by the same moth for defense.[9]

The different defense mechanisms have been shown to be directly responsive to bat echolocation through sympatry 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 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.[6] 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.[10]

Some bats are known to use clicks at frequencies above or below moths' hearing ranges.[8] 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.[11] Barbastelle 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.[8] The lower volume of clicks reduces the effective successful hunting range, but results in a significantly higher number of moths caught than other, louder bat species.[8][12] 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.[8] This allows them to decide whether or not defensive ultrasonic clicks are worth the time and energy expenditure.[13]

The rough-skinned newt and the common garter snake

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Rough-skinned newt

Rough-skinned newts have skin glands that contain a powerful nerve poison, tetrodotoxin, as an anti-predator adaptation. Throughout much of the newt's range, the common garter snake 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, 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.[14][15][16]

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.[17] While isolated garter snakes have lower resistance, they still demonstrate an ability to resist low levels of the toxin, suggesting an ancestral predisposition to tetrodotoxin resistance.[18][19] 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.[17] The same pattern is seen in isolated populations of newts, which have less toxin in their skin.[20] There are geographic hotspots where levels of tetrodotoxin and resistance are extremely high, showing a close interaction between newts and snakes.[17]

Predator whelk and the hard-shelled bivalve prey

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The whelk 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 who were more efficient at opening the larger-shelled prey.[21] 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.

Floodplain death adders and separate species of frogs

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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 overcome the chemical defenses of the toxic frogs after their death.[22] 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.[22] The coevolution is still highly asymmetrical because of the advantage the predators have over their prey.[22]

Introduced species

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Cane Toads have experienced a massive population explosion in Australia due to the lack of competition.

When a species has not been subject to an arms race previously, it may be at a severe disadvantage and face extinction 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 Australia or the Hawaiian Islands. In Australia, many invasive species, such as cane toads and rabbits, have spread rapidly due to a lack of competition and a lack of adaptations to cane toad bufotenine on the part of potential predators. Introduced species are a major reason why some indigenous species become endangered or even extinct, as was the case with the dodo.[citation needed]

See also

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References

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  1. ^ Dawkins, R. 1996. The Blind Watchmaker New York: W. W. Norton. Note: This book was also published by Penguin in 1991. While the text is identical, page numbers differ
  2. ^ Thierry Lodé "La guerre des sexes chez les animaux" Eds Odile Jacob, Paris ISBN 2-7381-1901-8;
  3. ^ da Cruz, João Filipe; Gaspar, Helena; Calado, Gonçalo (29 November 2011). "Turning the game around: toxicity in a nudibranch-sponge predator–prey association". Chemoecology. 22 (1): 47–53. doi:10.1007/s00049-011-0097-z. S2CID 17819241.
  4. ^ Van Valen, Leigh (1973). A new evolutionary law, Evolutionary Theory 1, 1¬30
  5. ^ Flier, W. G.; Turkensteen, L. J.; van den Bosch, G. B. M.; Vereijken, P. F. G.; Mulder, A. (2001). "Differential interaction of Phytophthora infestans on tubers of potato cultivars with different levels of blight resistance". Plant Pathology. 50 (3): 292–301. doi:10.1046/j.1365-3059.2001.00574.x. ISSN 0032-0862.
  6. ^ a b Fullard, J. H.; Ratcliffe, J. M.; Soutar, A. R. (2004). "Extinction of the acoustic startle response in moths endemic to a bat-free habitat". Journal of Evolutionary Biology. 17 (4): 856–861. doi:10.1111/j.1420-9101.2004.00722.x. PMID 15271085. S2CID 1054325.
  7. ^ Miller, Lee A.; Surlykke, Annemarie (July 2001). "How Some Insects Detect and Avoid Being Eaten by Bats: Tactics and Countertactics of Prey and Predator" (PDF). BioScience. 51 (7): 570–581. doi:10.1641/0006-3568(2001)051[0570:HSIDAA]2.0.CO;2. Evolutionarily speaking, insects have responded to selective pressure from bats with new evasive mechanisms[...]
  8. ^ a b c d e Palmer, Jason (19 August 2010). "Bat and moth arms race revealed". BBC News.
  9. ^ a b Yager, D. D. (2012). "Predator detection and evasion by flying insects". Current Opinion in Neurobiology. 22 (2): 201–207. doi:10.1016/j.conb.2011.12.011. PMID 22226428. S2CID 24365000.
  10. ^ Muma, K. E.; Fullard, J. H. (2004). "Persistence and regression of hearing in the exclusively diurnal moths, Trichodezia albovittata (Geometridae) and Lycomorpha pholus (Arctiidae)". Ecological Entomology. 29 (6): 718–726. Bibcode:2004EcoEn..29..718M. doi:10.1111/j.0307-6946.2004.00655.x. S2CID 83732973.
  11. ^ Waters, D. A. (2003). "Bats and moths: what is there left to learn?". Physiological Entomology. 28 (4): 237–250. doi:10.1111/j.1365-3032.2003.00355.x. S2CID 86269745.
  12. ^ Goerlitz, Holger R.; ter Hofstede, Hannah M.; Zeale, Matt R. K.; Jones, Gareth; Holderied, Marc W. (2010). "An Aerial-Hawking Bat Uses Stealth Echolocation to Counter Moth Hearing". Current Biology. 20 (17): 1568–1572. Bibcode:2010CBio...20.1568G. doi:10.1016/j.cub.2010.07.046. PMID 20727755.
  13. ^ Ratcliffe, John M.; Fullard, James H.; Arthur, Benjamin J.; Hoy, Ronald R. (2010). "Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats". Proceedings of the Royal Society B: Biological Sciences. 278 (1704): 364–370. doi:10.1098/rspb.2010.1488. PMC 3013417. PMID 20719772. Open access icon
  14. ^ Feldman, C. R.; Brodie, E. D.; Brodie, E. D.; Pfrender, M. E. (2009). "The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly pre". PNAS. 106 (32): 13415–13420. Bibcode:2009PNAS..10613415F. doi:10.1073/pnas.0901224106. PMC 2726340. PMID 19666534.
  15. ^ Hanifin, Charles T. (2010). "The Chemical and Evolutionary Ecology of Tetrodotoxin (TTX) Toxicity in Terrestrial Vertebrates". Marine Drugs. 8 (3): 577–593. doi:10.3390/md8030577. PMC 2857372. PMID 20411116.
  16. ^ Feldman, C. R.; Brodie, E. D.; Brodie, E. D.; Pfrender, M. E. (2010). "Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey". Proceedings of the Royal Society B: Biological Sciences. 277 (1698): 3317–3325. doi:10.1098/rspb.2010.0748. PMC 2981930. PMID 20522513.
  17. ^ a b c 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". Evolution. 56 (10): 2067–82. doi:10.1554/0014-3820(2002)056[2067:teropt]2.0.co;2. PMID 12449493. S2CID 8251443.
  18. ^ Brodie, Edmund D.; Brodie, Edmund D. Jr.; Motychak, Jeffrey E. (2002). "Recovery of garter snakes (Thamnophis sirtalis) from the effects of tetrodotoxin. Hpet". Journal of Herpetology. 36 (1): 95–98. doi:10.2307/1565808. JSTOR 1565808.
  19. ^ 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". Journal of Chemical Ecology. 31 (2): 343–356. Bibcode:2005JCEco..31..343B. doi:10.1007/s10886-005-1345-x. PMID 15856788. S2CID 16542226.
  20. ^ 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". Evolution. 45 (1): 221–224. doi:10.2307/2409496. JSTOR 2409496. PMID 28564068.
  21. ^ Dietl, Gregory P. (3 November 2003). "Coevolution of a marine gastropod predator and its dangerous bivalve prey". Biological Journal of the Linnean Society. 80 (3): 409–436. doi:10.1046/j.1095-8312.2003.00255.x.
  22. ^ a b c Phillips, Ben; Shine, Richard (December 2007). "When Dinner Is Dangerous: Toxic Frogs Elicit Species-Specific Responses from a Generalist Snake Predator". The American Naturalist. 170 (6): 936–942. doi:10.1086/522845. PMID 18171175. S2CID 9744969.

General

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