Experimental immune challenges reduce the quality of male antennae and female pheromone output

Hieu T Pham,Kathryn B Mcnamara,Emile Van Lieshout,Mark A Elgar

doi:10.1038/s41598-022-07100-y

Hieu T Pham, Kathryn B Mcnamara + Show 2 more

Open Access

https://doi.org/10.1038/s41598-022-07100-y

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Abstract

Sexual signalling is a key feature of reproductive investment, yet the effects of immune system activation on investment into chemical signalling, and especially signal receiver traits such as antennae, are poorly understood. We explore how upregulation of juvenile immunity affects male antennal functional morphology and female pheromone attractiveness in the gumleaf skeletonizer moth, Uraba lugens. We injected final-instar larvae with a high or low dose of an immune elicitor or a control solution and measured male antennal morphological traits, gonad investment and female pheromone attractiveness. Immune activation affected male and female signalling investment: immune challenged males had a lower density of antennal sensilla, and the pheromone of immune-challenged females was less attractive to males than their unchallenged counterparts. Immune challenge affected female investment into ovary development but not in a linear, dose-dependent manner. While there was no effect of immune challenge on testes size, there was a trade-off between male pre- and post-copulatory investment: male antennal length was negatively correlated with testes size. Our study highlights the costs of elaborate antennae and pheromone production and demonstrates the capacity for honest signalling in species where the costs of pheromone production were presumed to be trivial.

Highlights

Sexual signalling is a key feature of reproductive investment, yet the effects of immune system activation on investment into chemical signalling, and especially signal receiver traits such as antennae, are poorly understood
Our experiments demonstrate that immune investment impacts pre- and post-copulatory reproductive investment and life-history traits in both male and female gumleaf skeletonizer moths, but not in a consistently dosedependent manner
Our novel results demonstrate that chemical communication is costly for both males and females: immune trade-offs affect male sensory structures, highlighting the costs of elaborate antennae, and the attractiveness of the female pheromone declines following immune challenge

Summary

Introduction

Sexual signalling is a key feature of reproductive investment, yet the effects of immune system activation on investment into chemical signalling, and especially signal receiver traits such as antennae, are poorly understood. We explore how upregulation of juvenile immunity affects male antennal functional morphology and female pheromone attractiveness in the gumleaf skeletonizer moth, Uraba lugens. Immune activation affected male and female signalling investment: immune challenged males had a lower density of antennal sensilla, and the pheromone of immunechallenged females was less attractive to males than their unchallenged counterparts. Trade-offs between immune investment and chemical-receiving structures (antennae) have not been examined, despite the costs of maintaining these structures[21,22] and their obvious role in reproduction through mate location and reception of sensory information used in mate assessment. In the Lepidoptera, female moths release minute quantities of sex-pheromone[26,27], so selection may favour males with antennal morphology, including antennal length and sensilla numbers, that optimises odorantreceptor interactions[24,28,29]. Barthel et al.[16] provide rare evidence of a trade-off between female sex pheromone and immunity: the composition of sex pheromone produced by female tobacco budworm moths, Heliothis virescens, changed following injection with a pathogenic immune elicitor, with females experiencing reduced mating success

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