Genetic architecture facilitates then constrains adaptation in a host-parasite coevolutionary arms race.
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Authors
Spottiswoode, Claire N
Tong, Wenfei
Stryjewski, Katherine F
DaCosta, Jeffrey M
Kuras, Evan R
Green, Ailsa
Hamama, Silky
Taylor, Ian G
Moya, Collins
Publication Date
2022-04-26Journal Title
Proc Natl Acad Sci U S A
ISSN
0027-8424
Publisher
Proceedings of the National Academy of Sciences
Type
Article
This Version
AM
Metadata
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Spottiswoode, C. N., Tong, W., Jamie, G. A., Stryjewski, K. F., DaCosta, J. M., Kuras, E. R., Green, A., et al. (2022). Genetic architecture facilitates then constrains adaptation in a host-parasite coevolutionary arms race.. Proc Natl Acad Sci U S A https://doi.org/10.1073/pnas.2121752119
Abstract
In coevolutionary arms races, interacting species impose selection on each other, generating reciprocal adaptations and counter adaptations. This process is typically enhanced by genetic recombination and heterozygosity, but these sources of evolutionary novelty may be secondarily lost when uniparental inheritance evolves to ensure the integrity of sex-linked adaptations. We demonstrate that host-specific egg mimicry in the African cuckoo finch Anomalospiza imberbis is maternally inherited, confirming the validity of an almost century-old hypothesis. We further show that maternal inheritance not only underpins the mimicry of different host species but also additional mimetic diversification that approximates the range of polymorphic egg “signatures” that have evolved within host species as an escalated defense against parasitism. Thus, maternal inheritance has enabled the evolution and maintenance of nested levels of mimetic specialization in a single parasitic species. However, maternal inheritance and the lack of sexual recombination likely disadvantage cuckoo finches by stifling further adaptation in the ongoing arms races with their individual hosts, which we show have retained biparental inheritance of egg phenotypes. The inability to generate novel genetic combinations likely prevents cuckoo finches from mimicking certain host phenotypes that are currently favored by selection (e.g., the olive-green colored eggs laid by some tawny-flanked prinia, Prinia subflava, females). This illustrates an important cost of coding coevolved adaptations on the nonrecombining sex chromosome, which may impede further coevolutionary change by effectively reversing the advantages of sexual reproduction in antagonistic coevolution proposed by the Red Queen hypothesis.
Sponsorship
BBSRC David Research Fellowship (BB/J014109/1)
Royal Society Dorothy Hodgkin Fellowship
DST-NRF Centre of Excellence at the FitzPatrick Institute
NSF (DEB 0640759)
Funder references
Biotechnology and Biological Sciences Research Council (BB/J014109/1)
The Royal Society (dh0867528)
Royal Society (RG2010/RZ)
Identifiers
External DOI: https://doi.org/10.1073/pnas.2121752119
This record's URL: https://www.repository.cam.ac.uk/handle/1810/334070
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