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dc.contributor.author
Müller, Viktor
dc.contributor.author
de Boer, Rob J.
dc.contributor.author
Bonhoeffer, Sebastian
dc.contributor.author
Szathmáry, Eörs
dc.date.accessioned
2018-04-10T13:07:43Z
dc.date.available
2018-01-25T07:29:12Z
dc.date.available
2018-01-30T13:06:06Z
dc.date.available
2018-04-10T13:07:43Z
dc.date.issued
2018-02
dc.identifier.other
10.1111/brv.12355
en_US
dc.identifier.uri
http://hdl.handle.net/20.500.11850/234046
dc.identifier.doi
10.3929/ethz-b-000234046
dc.description.abstract
We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function‐based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to ‘learn’ by cumulative trial‐and‐error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher‐level units entail the suppression of selection at lower levels, Darwinian immunity re‐opens cell‐level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell‐level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re‐invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system – the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the ‘Big Bang’ of vertebrate immunity, arguing that its origin involved a ‘difficult’ (i.e. low‐probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.
en_US
dc.format
application/pdf
en_US
dc.language.iso
en
en_US
dc.publisher
Wiley-Blackwell
en_US
dc.rights.uri
http://creativecommons.org/licenses/by/4.0/
dc.subject
major evolutionary transition
en_US
dc.subject
adaptive immunity
en_US
dc.subject
Darwinian immunity
en_US
dc.subject
Lamarckian immunity
en_US
dc.subject
shotgun immunity
en_US
dc.subject
evolutionary scenario
en_US
dc.title
An evolutionary perspective on the systems of adaptive immunity
en_US
dc.type
Journal Article
dc.rights.license
Creative Commons Attribution 4.0 International
dc.date.published
2017-07-26
ethz.journal.title
Biological Reviews
ethz.journal.volume
93
en_US
ethz.journal.issue
1
en_US
ethz.pages.start
505
en_US
ethz.pages.end
528
en_US
ethz.version.deposit
publishedVersion
en_US
ethz.identifier.wos
ethz.publication.place
Oxford
en_US
ethz.publication.status
published
en_US
ethz.leitzahl
ETH Zürich::00002 - ETH Zürich::00012 - Lehre und Forschung::00007 - Departemente::02350 - Dep. Umweltsystemwissenschaften / Dep. of Environmental Systems Science::02720 - Institut für Integrative Biologie / Institute of Integrative Biology::03584 - Bonhoeffer, Sebastian / Bonhoeffer, Sebastian
en_US
ethz.leitzahl.certified
ETH Zürich::00002 - ETH Zürich::00012 - Lehre und Forschung::00007 - Departemente::02350 - Dep. Umweltsystemwissenschaften / Dep. of Environmental Systems Science::02720 - Institut für Integrative Biologie / Institute of Integrative Biology::03584 - Bonhoeffer, Sebastian / Bonhoeffer, Sebastian
en_US
ethz.date.deposited
2018-01-25T07:29:12Z
ethz.source
FORM
ethz.eth
yes
en_US
ethz.availability
Open access
en_US
ethz.rosetta.installDate
2018-04-10T13:07:47Z
ethz.rosetta.lastUpdated
2018-11-06T17:42:53Z
ethz.rosetta.versionExported
true
ethz.COinS
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