Parental investment and immune dynamics in sex-role reversed pipefishes

Abstract

27Parental care elevates reproductive success by allocating resources into the 28 upbringing of the offspring. However, it also imposes strong costs for the care giving 29 parent and can foster sexual dimorphism. Trade-offs between the reproductive system 30 and the immune system may result in differential immunological capacities between 31 the care-providing and the non-care-providing parent. Usually, providing care is 32 restricted to the female sex making it impossible to study a sex-independent influence 33 of parental investment on sexual immune dimorphism. The decoupling of sex-34 dependent parental investment and their influences on the parental immunological 35 capacity, however, is possible in syngnathids, which evolved the unique male 36 pregnancy on a gradient ranging from a simple carrying of eggs on the trunk 37 (Nerophinae, low paternal investment) to full internal pregnancy (Syngnathus, high 38 paternal investment). In this study, we compared candidate gene expression between 39 females and males of different gravity stages in three species of syngnathids 40 (Syngnathus typhle, Syngnathus rostellatus and Nerophis ophidion) with different male 41 pregnancy intensities to determine how parental investment influences sexual immune 42 dimorphism. While our data failed to detect sexual immune dimorphism in the subset 43 of candidate genes assessed, we show a parental care specific resource-allocation 44 trade-off between investment into pregnancy and immune defense when parental care 45 is provided. 46 47 48 49 3 50 Introduction: 51 Sex-specific life histories have evolved as a consequence of anisogamy; females 52 contribute the large costly eggs and males provide the always available small sperm 53 to reproduction. To gain access to females and to maximize reproductive success, 54 males need to allocate their resources into male-male competition and the display of 55 secondary sexual signals. In contrast, females are striving for longevity to maximize 56 their lifetime reproductive success, which requires a higher investment into pathogen 57 defense (1-5). Females were thus suggested to having a more efficient immune 58 system than males (6). 59 Distinct life-history strategies between males and females can also result in differing 60 investment into the upbringing of the offspring, i.e. parental care. Parental care 61 elevates reproductive success by increasing offspring survival, however, it also 62 reduces prospects of future reproduction of the care providing parent due to a trade-63 off between investment in offspring and investment into other fitness-related traits (7). 64 This can foster sexual dimorphism (8-12) and might also contribute to sexual immune 65 dimorphism (13,14). To understand how parental care impacts sexual immune 66 dimorphism, the comparison of closely related species that differ in their provisioning 67 of parental care is essential. 68 Syngnathids, the teleost family of seahorses and pipefishes, with their unique male 69 pregnancy, represent an ideal model system to assess t...

Immunological tolerance in the evolution of male pregnancy

“…Male immune capabilities are higher than in female syngnathids but have been shown to come at a cost during pregnancy (Lin et al, 2016; Roth et al, 2011). Immune system states of pouch bearing syngnathids fluctuate owing to the shifting foeto‐paternal demands, and a consensus is growing that immune modulation is present and necessary (Keller & Roth, 2020; Li et al, 2020; Roth et al, 2020; Whittington et al, 2015). These observations are extended here in all pouched species, with many adaptive immune genes charged with tasks in antigen presentation and processing, showing a downregulation predominantly during early gestation (Table ).…”

“…Syngnathid research has highlighted genetic and morphological congruencies found between male and eutherian mammal reproductive systems (Roth et al, 2020; Small et al, 2013; Stölting & Wilson, 2007; Whittington et al, 2015), with special interest being funnelled into immunological and nutrient transfer processes (Beemelmanns et al, 2019; Beemelmanns & Roth, 2017; Ripley & Foran, 2009; Roth et al, 2012, 2020; Skalkos et al, 2020). Similarly, several studies have characterised brood pouch tissue gene expression at multiple pregnancy stages in Hippocampus abdominalis (Lin et al, 2017; Whittington et al, 2015) and more recently two Syngnathus species (Keller & Roth, 2020; Roth et al, 2020; Small et al, 2013), showing transcriptional changes in pathway processes such as tissue remodelling, nutrient transport and immunity. The functional absence of MHC II pathway components in some pouch bearing syngnathids ( Syngnathus and Hippocampus (Haase et al, 2013; Luo et al, 2016; Roth et al, 2020) has stimulated discussions about the loss's potential immune modulatory role in the evolution of advanced paternal pregnancy.…”