Male Pregnancy and Biparental Immune Priming

Abstract

In vertebrates, maternal transfer of immunity via the eggs or placenta provides offspring with crucial information on prevailing pathogens and parasites. Males contribute little to such transgenerational immune priming, either because they do not share the environment and parasite pressure of the offspring or because sperm are too small for transfer of immunity. In the teleost group of Syngnathids (pipefish, seahorses, and sea dragons), males brood female eggs in a placenta-like structure. Such sex-role-reversed species provide a unique opportunity to test for adaptive plasticity in immune transfer. Here, males and females should both influence offspring immunity. We experimentally tested paternal effects on offspring immunity by examining immune cell proliferation and immune gene expression. Maternal and paternal bacterial exposure induced offspring immune defense 5 weeks after hatching, and this effect persisted in 4-month-old offspring. For several offspring immune traits, double parental exposure (maternal and paternal) enhanced the response, whereas for another group of immune traits, the transgenerational induction already took place if only one parent was exposed. Our study shows that sex role reversal in connection with male pregnancy opens the door for biparental influences on offspring immunity and may represent an additional advantage for the evolution of male pregnancy.

Experimental evidence that parasites drive eco-evolutionary feedbacks

“…In this case, the regulatory response of juveniles may reflect the stronger parasite resistance of stream sticklebacks. In natural populations, the translation of parasite effects across generations, mediated by host-modified ecosystems, might be combined with transgenerational immune priming when hosts inherit epigenetic signals of their parents' previous infections (36,48). However, we can rule out this possibility in our experiment because juveniles were not the direct offspring of phase 1 adults.…”

Eco-Evolutionary Dynamics

“…Isaksson et al, 2006) and transmission of immune factors (e.g. Jacquin et al, 2012;Roth et al, 2012) exist in the literature. In addition, females can alter their investment in offspring in response to males' characteristics (e.g.…”

Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring

“…Exceptional cases are sex-role-reversed species like pipefish, seahorses and sea dragons which provide a unique opportunity to test for adaptive plasticity in parental immune transfer. Here, males and females both influence offspring immunity [17]. Paternal effects influencing the immune system of offspring are rarely documented in vertebrates [18], however, there is growing evidence in insects [6–8,11,19–24].…”