Sperm success and immunity

Abstract

The moment of the fertilization of an egg by a spermatozoon-the point of "sperm success"-is a key milestone in the biology of sexually reproducing species and is a fundamental requirement for offspring production. Fertilization also represents the culmination of a suite of sexually selected processes in both sexes and is commonly used as a landmark to measure reproductive success. Sperm success is heavily dependent upon interactions with other key aspects of male and female biology, with the immune system among the most important. The immune system is vital to maintaining health in both sexes; however, immune reactions can also have antagonistic effects on sperm success. The effects of immunity on sperm success are diverse, and may include trade-offs in the male between investment in the production or protection of sperm, as well as more direct, hostile, immune responses to sperm within the female, and potentially the male, reproductive tract. Here, we review current understanding of where the biology of immunity and sperm meet, and identify the gaps in our knowledge.

Differential gene regulation in selected lines for high and low sperm production in male guppies

“…A higher investment in sperm production was associated with a downregulation of pathways related to immunity and with a downregulation of pathways related to the control of cell cycles, DNA damage and mitochondrial enzyme activity. Altogether, these results suggest that producing high sperm numbers may come at a cost for immunocompetence, in accordance with the hypothesized trade‐off between sexually‐selected traits and immunity (reviewed in Wigby et al, 2019). This cost may impose a limit on sperm investment explaining the strong stabilizing selection on sperm number observed in these artificially selected lines after removing artificial selection (Cattelan et al, 2018).…”

“…For example, the glial cell line‐derived neurotrophic factor is a known cytokine that promotes the proliferation of cells and it is crucial in regulating the proliferation and renewal of spermatogonial cells (Zhu, Yang, & Li, 2015). The cost of sperm production may come from concurrent immunosuppression and therefore an increase in sperm production could be traded off with immunity (Wigby, Suarez, Lazzaro, Pizzari, & Wolfner, 2019).…”

Molecular insights into post‐mating immune response in a fish with internal fertilization

“…Indeed, although this may be true in some species, the universality of this ‘pre‐emptive strike’ response (Peng, Zipperlen, & Kubli, 2005) has been recently challenged by several studies showing that the components of the ejaculate (sperm and seminal fluid) are immunogenic to females (Lawniczak et al, 2007; Morrow & Innocenti, 2012). Moreover, although the activation of an immune response by females after mating has been reported in many species (Johansson, Bromfield, Jasper, & Robertson, 2004; Robertson, 2005; Wigby, Suarez, Lazzaro, Pizzari, & Wolfner, 2019), in other species the opposite occurs, and mating has instead an immune suppressant effect on females (Fedorka & Zuk, 2005; McKean & Nunney, 2001; Oku, Price, & Wedell, 2019; Rolff & Siva‐Jothy, 2002). Interpreting this down‐regulation of the immune function (or part thereof) triggered by mating invokes different, nonmutually exclusive, explanations.…”

“…Despite recent developments in the field, we still lack basic knowledge of the molecular mechanisms of the female post‐mating immune response in many species and even in entire taxa. Studying whether and to what extent the female immune system is engaged by the reproductive event is indeed important for our understanding of basic mechanisms of reproduction but also of mechanisms of sexual selection such as cryptic female choice (where the female can bias fertilization towards the preferred male, Eberhard, 1996), sperm competition (where sperm from two or more males compete to fertilize the same set of eggs, Parker, 1970) and sexual conflict (Arnqvist & Rowe, 2005; Parker, 1979), to ultimately understand whether and how immunity is associated to mechanisms of post‐mating sexual selection (Wigby et al, 2019).…”

Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics

“…Maintaining the long-term viability of sperm presents challenges [7]. Without 33 protection, stored sperm are at risk of desiccation, thermal stress, immune attack, and the 34 mutagenic action of oxidative stress.…”