Interactions between immune cell types facilitate the evolution of immune traits

Tania Dubovik, Martin Lukačišin, Elina Starosvetsky, Benjamin LeRoy, Rachelly Normand, Yasmin Admon, Ayelet Alpert, Yishai Ofran, Max G’Sell and Shai S. Shen-Orr ()
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Tania Dubovik: Faculty of Medicine, Technion – Israel Institute of Technology
Martin Lukačišin: Faculty of Medicine, Technion – Israel Institute of Technology
Elina Starosvetsky: Faculty of Medicine, Technion – Israel Institute of Technology
Benjamin LeRoy: Carnegie Mellon University
Rachelly Normand: Faculty of Medicine, Technion – Israel Institute of Technology
Yasmin Admon: Faculty of Medicine, Technion – Israel Institute of Technology
Ayelet Alpert: Faculty of Medicine, Technion – Israel Institute of Technology
Yishai Ofran: Faculty of Medicine, Technion – Israel Institute of Technology
Max G’Sell: Carnegie Mellon University
Shai S. Shen-Orr: Faculty of Medicine, Technion – Israel Institute of Technology

Nature, 2024, vol. 632, issue 8024, 350-356

Abstract: Abstract An essential prerequisite for evolution by natural selection is variation among individuals in traits that affect fitness1. The ability of a system to produce selectable variation, known as evolvability2, thus markedly affects the rate of evolution. Although the immune system is among the fastest-evolving components in mammals3, the sources of variation in immune traits remain largely unknown4,5. Here we show that an important determinant of the immune system’s evolvability is its organization into interacting modules represented by different immune cell types. By profiling immune cell variation in bone marrow of 54 genetically diverse mouse strains from the Collaborative Cross6, we found that variation in immune cell frequencies is polygenic and that many associated genes are involved in homeostatic balance through cell-intrinsic functions of proliferation, migration and cell death. However, we also found genes associated with the frequency of a particular cell type that are expressed in a different cell type, exerting their effect in what we term cyto-trans. The vertebrate evolutionary record shows that genes associated in cyto-trans have faced weaker negative selection, thus increasing the robustness and hence evolvability2,7,8 of the immune system. This phenomenon is similarly observable in human blood. Our findings suggest that interactions between different components of the immune system provide a phenotypic space in which mutations can produce variation with little detriment, underscoring the role of modularity in the evolution of complex systems9.

Date: 2024
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DOI: 10.1038/s41586-024-07661-0

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