Vive la difference! Self/non-self recognition and the evolution of signatures of identity in arms races with parasites

TY - JOUR

T1 - Vive la difference!

T2 - Self/non-self recognition and the evolution of signatures of identity in arms races with parasites

AU - Spottiswoode, Claire

AU - Busch, Robert

N1 - Please note that this was a contribution to a special issue of the journal. For reasons beyond my control, this ms. was not made Open Access. I will therefore keep the accepted version on file here. This is not primary research, so I will not nominate for REF.

PY - 2019/2/11

Y1 - 2019/2/11

N2 - In arms races with parasites, hosts can evolve defences exhibiting extensive variability within populations, which signals individual identity (“signatures”). However, few such systems have evolved, suggesting that the conditions for their evolution are uncommon. We review (a) polymorphic egg markings that allow hosts of brood-parasitic birds to recognise and reject parasitic eggs, and (b) polymorphic tissue antigens encoded in the major histocompatibility complex (MHC), which present self- and pathogen-derived peptides to T cells of the immune system. Despite the profound differences between these systems, they share analogous features: (i) self/non-self discrimination by a highly specific recognition system (bird eyes and T-cell antigen receptor, respectively), which antagonists may escape by evolving evasion or mimicry; (ii) a self substrate upon which diversifying selection can act (eggs, and MHC molecules); (iii) acquired knowledge of self (resulting in acceptance of own eggs, and immune tolerance), and (iv) fitness costs associated with attack on self or lack of parasite detection. We suggest that these features comprise a set of requirements for parasites to drive the evolution of identity signatures in hosts, which diminish the likelihood of recognition errors. This may help to explain the variety of trajectories arising from arms races in different antagonistic contexts.© 2018, The Author(s), published by The Royal Society. This is an author produced version of a paper published in PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B: BIOLOGICAL SCIENCES uploaded in accordance with the publisher’s self- archiving policy. The final published version (version of record) is available online at the link below. Some minor differences between this version and the final published version may remain. We suggest you refer to the final published version should you wish to cite from it.

AB - In arms races with parasites, hosts can evolve defences exhibiting extensive variability within populations, which signals individual identity (“signatures”). However, few such systems have evolved, suggesting that the conditions for their evolution are uncommon. We review (a) polymorphic egg markings that allow hosts of brood-parasitic birds to recognise and reject parasitic eggs, and (b) polymorphic tissue antigens encoded in the major histocompatibility complex (MHC), which present self- and pathogen-derived peptides to T cells of the immune system. Despite the profound differences between these systems, they share analogous features: (i) self/non-self discrimination by a highly specific recognition system (bird eyes and T-cell antigen receptor, respectively), which antagonists may escape by evolving evasion or mimicry; (ii) a self substrate upon which diversifying selection can act (eggs, and MHC molecules); (iii) acquired knowledge of self (resulting in acceptance of own eggs, and immune tolerance), and (iv) fitness costs associated with attack on self or lack of parasite detection. We suggest that these features comprise a set of requirements for parasites to drive the evolution of identity signatures in hosts, which diminish the likelihood of recognition errors. This may help to explain the variety of trajectories arising from arms races in different antagonistic contexts.© 2018, The Author(s), published by The Royal Society. This is an author produced version of a paper published in PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B: BIOLOGICAL SCIENCES uploaded in accordance with the publisher’s self- archiving policy. The final published version (version of record) is available online at the link below. Some minor differences between this version and the final published version may remain. We suggest you refer to the final published version should you wish to cite from it.

KW - Evolutionary ecology, host-parasite arms races, balanced polymorphism, 19 negative frequency-dependent selection, avian egg pattern diversification, brood parasites, 20 immunology, major histocompatibility complex, T-cell antigen presentation

U2 - 10.1098/rstb.2018.0206

DO - 10.1098/rstb.2018.0206

M3 - Article

SN - 0962-8436

VL - 374

JO - PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES

JF - PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES

M1 - 20180206

ER -