Parental investment and immune dynamics in sex-role reversed pipefishes

Abstract

Parental care elevates reproductive success by allocating resources into the upbringing of the offspring. However, it also imposes strong costs for the care-giving parent and can foster sexual dimorphism. Trade-offs between the reproductive system and the immune system may result in differential immunological capacities between the care-providing and the noncare-providing parent. Usually, providing care is restricted to the female sex making it impossible to study a sex-independent influence of parental investment on sexual immune dimorphism. The decoupling of sex-dependent parental investment and their influences on the parental immunological capacity, however, is possible in syngnathids, which evolved the unique male pregnancy on a gradient ranging from a simple carrying of eggs on the trunk (Nerophinae, low paternal investment) to full internal pregnancy (Syngnathus, high paternal investment). In this study, we compared candidate gene expression between females and males of different gravity stages in three species of syngnathids (Syngnathus typhle, Syngnathus rostellatus and Nerophis ophidion) with different male pregnancy intensities to determine how parental investment influences sexual immune dimorphism. While our data failed to detect sexual immune dimorphism in the subset of candidate genes assessed, we show a parental care specific resource-allocation trade-off between investment into pregnancy and immune defense when parental care is provided.

Immunological tolerance in the evolution of male pregnancy

“…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, 2012Roth et al, , 2020Skalkos et al, 2020). Similarly, F I G U R E 1 Syngnathid brooding types: Nerophis ophidion (external egg-gluing/pregnancy), Syngnathus typhle (inverted brood pouch) and Hippocampus erectus (sealed brood pouch) 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.…”

Navigating sex and sex roles: deciphering sex-biased gene expression in a species with sex-role reversal (Syngnathus typhle)

“…Interestingly, pregnancy exhibited minimal or no effect on gene expression across all examined organs. This observation suggests that the physiological changes associated with pregnancy may not significantly affect the selected organs, considering that another study comparing pouch tissues and pregnancy gradients across four different syngnathid species found DEGs in immune pathways and metabolic processes (58,59).…”

“…This broader repertoire of immune receptors could effectively recognize a wider array of pathogens. This divergence might reflect evolutionary adaptations that cater to distinct immune system demands between the two sexes (58). We know that sex-specific pathogens exist in other fish species due to sex-specific behaviours, such as shoaling behaviour in female guppies' increased ectoparasite loads (77).…”

Genome rearrangements, male pregnancy and immunological tolerance – the curious case of the syngnathid immune system

“…MHC I pathway related downregulation was found to occur specifically during early gestation in syngnathids with a defined brood pouch, contrary to pouchless species . Immunological activity differences between brooding strategies have also been observed in S. typhle (inverted brood pouch), which exhibited a greater immune investment during pregnancy compared with Nerophis ophidion (pouchless) (Keller and Roth, 2020). These reports suggest that the evolution of the more 'intimate' brooding strategies required the coevolution of immune suppressive measures to accommodate the progeny.…”

“…Recent discoveries have highlighted the occurrence of adaptive immune system remodelling in some pipefish and seahorse species, giving rise to a convoluted and drastically alternative set of immune defences (Bahr and Wilson, 2011;Haase et al, 2013;Roth et al, 2020). Alongside and succeeding these studies, research has delved further into the molecular underpinnings that shaped these enigmatic fish defences; exploring the links with male pregnancy evolution, immunological tolerance, transgenerational immune priming and alternative immune strategies (Figure 1) Whittington et al, 2015;Beemelmanns and Roth, 2016a;Keller and Roth, 2020;Whittington and Friesen, 2020;. This review attempts to summarise the growing body of research concerning the syngnathid immune system, its evolution, and associations with other facets of their physiology and reproduction.…”