Abstract

Both the brain and the immune system are energetically demanding organs, and when natural selection favours increased investment into one, then the size or performance of the other should be reduced. While comparative analyses have attempted to test this potential evolutionary trade-off, the results remain inconclusive. To test this hypothesis, we compared the tissue graft rejection (an assay for measuring innate and acquired immune responses) in guppies (Poecilia reticulata) artificially selected for large and small relative brain size. Individual scales were transplanted between pairs of fish, creating reciprocal allografts, and the rejection reaction was scored over 8 days (before acquired immunity develops). Acquired immune responses were tested two weeks later, when the same pairs of fish received a second set of allografts and were scored again. Compared with large-brained animals, small-brained animals of both sexes mounted a significantly stronger rejection response to the first allograft. The rejection response to the second set of allografts did not differ between large- and small-brained fish. Our results show that selection for large brain size reduced innate immune responses to an allograft, which supports the hypothesis that there is a selective trade-off between investing into brain size and innate immunity.

Highlights

  • Organisms do not have unlimited resources and when natural selection favours increased investment into one trait, there are fewer resources to invest into other traits [1]

  • The first set of allografts, used to assay innate immunity, elicited a stronger rejection response than the second set of allografts, used to measure adaptive immunity; small-brained fish and males tended to show a stronger rejection response than large-brained fish and females; we further found a significant interaction between brain-size selection regime and set of allograft (GLMM1: allograft set: F1,394 1⁄4 127.302, p, 0.001; sex: F1,56 1⁄4 3.608, p 1⁄4 0.063; brain-size selection regime: F1,56 1⁄4 3.608, p 1⁄4 0.063; day of experiment: F1,395 1⁄4 44.253, p, 0.001; day of experiment2: F1,395 1⁄4 3.188, p 1⁄4 0.075; allograft set  brain-size selection regime: F1,402 1⁄4 3.932, p 1⁄4 0.048; figure 1)

  • We found that small-brained animals mounted a significantly stronger rejection response to first-set allografts than did large-brained animals

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Summary

Introduction

Organisms do not have unlimited resources and when natural selection favours increased investment into one trait, there are fewer resources to invest into other traits [1]. This limitation is the basis for life-history trade-offs, and can potentially restrict or bias evolutionary pathways [2,3,4,5]. It has long been assumed that large brain size imposes selective trade-offs with other traits. Identifying these selective trade-offs is vital for understanding brain evolution.

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