“Evolution of personal and social immunity in the context of parental care”

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Michelle A. Ziadie, Felicia Ebot-Ojong, Elizabeth C. McKinney, and Allen J. Moore (Feb 2019)

The DOI will be https://dx.doi.org/10.1086/701122

Social immunity involves specific genes and pathways reflecting evolution as an interacting phenotype during parenting

A mother Nicrophorus vespilloides feeding her begging babies.
(Credit: Allen J. Moore)

Offspring clearly benefit from parents providing food, but what if the parents and offspring live in a microbially rich environment? They might also benefit from parents transferring immunity, but how does this evolve? Is it generalized to all immune functions or is it directed to specific immune molecules? Michelle Ziadie, a PhD student in Moore’s laboratory in collaboration with an undergraduate, Felicia Ebot-Ojong, and research scientist, Libby McKinney, investigated this in a burying beetle. They used multiple experiments manipulating social conditions to distinguish between “social immunity” (where parents increase their immune gene expression specifically to help their offspring) and “shared personal immunity (where parents increase immune gene expression for themselves and offspring benefit indirectly). Burying beetles are especially suitable for this as the mother regurgitates predigested carrion to begging babies, and the parents and offspring live together on the dead vertebrate that they consume. Mothers use anal secretions to prevent the carrion from rotting, but given that they also directly feed their babies, there is an opportunity to transfer immunity to the offspring. Of the three genes studied, two influenced social immunity and one was involved in shared personal immunity. The gene involved in shared immunity is an anti-microbial peptide common in insects, defensing. The other two genes are more specialized, with pgrp-sc2 directly provisioned to babies and thaumatin specialized as an anti-fungal that is not found in insects. This suggests that social immunity provided by parents to offspring arises when the parents can provide directed and specialized immune protection.


Abstract

Social immunity moderates the spread of pathogens in social groups and is especially likely in groups structured by genetic relatedness. The extent to which specific immune pathways are used is unknown. Here, we investigate the expression and social role of three functionally separate immune genes (pgrp-sc2, thaumatin, and defensin) during parental care in the beetle Nicrophorus vespilloides. These genes reside in different immune pathways, allowing us to test if specific components of the immune system are targeted for social immunity. To test for the evolution of specificity we manipulated the influence of social context and timing on gene expression and quantified the covariance of maternal immune gene expression and offspring fitness. Larvae reduced expression of all three genes in the presence of parents. Parental pgrp-sc2 and thaumatin increased during direct parenting, while defensin was upregulated before larvae arrived. Parental expression of pgrp-sc2 and thaumatin responded similarly to experimental manipulation of timing and presence of larvae, which differed from the response of defensin. We found a positive covariance between maternal expression and offspring fitness for pgrp-sc2 and thaumatin, but not defensin. We suggest that social immunity can involve specific genes and pathways, reflecting evolution as an interacting phenotype during parenting.