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k Sexual Reproduction and Advanced article Article Contents Immunity • Introduction ⋆ • Reproductive Immunity Seth M Barribeau , Institute of Integrative Biology, University of Liverpool, • Three Selection Pressures Linking Reproduction Liverpool, UK and Immunity ⋆ • A Potential Regulation of the Link between Oliver Otti , University of Bayreuth, Bayreuth, Germany Reproduction and Immunity • Conclusion ⋆These authors contributed equally to this work. • Acknowledgements Online posting date: 20th July 2020 Sexual reproduction is a highly complicated pro- between males and females over the optimal reproductive invest- cess shaped in part by the need to optimise ment (Andersson, 1994). Antagonistic interests of the sexes led reproductive investment, which can differ and to fast-evolving and highly diverse reproductive traits in both evolve antagonistically between the sexes. Sex- sexes, of which male mating strategies and female pre-copulatory mate choice have been intensively studied (Andersson, 1994; ual reproduction is also intimately linked with Eberhard, 1996; Hosken and Stockley, 2004; Jennions and Petrie, immunity through a variety of means. Combining 1997). However, sexual reproduction can also increase the risk these seemingly disparate biological functions has of infection due to wounding and/or encounter probability of led to the emergence of the new field of repro- microbes. Protection against these infections demands resource ductive immunity. One striking parallel between investment in immunity, which, in turn, is a function of the host’s reproduction and immunity is the detection of physiological state (Adamo, 2008a,2008b; Westra et al., 2015) ‘other’. Failure to detect pathogens results in dis- and behaviour. ease. Failure to ignore self causes autoimmunity. There are three broad and likely co-occurring ways that immu- k Similarly, individuals, as well as gametes, must nity and reproduction might be connected. First, resources for any k choose appropriate partners avoiding interspecific individual are finite and thus must be allocated among all func- mating on one extreme or reproducing with kin tions, including immune defences and reproduction (reviewed in Schwenke et al., 2016). The rationale for this trade-off is to avoid inbreeding, on the other. The relation- intuitive; if immune defences increase, fewer resources are avail- ship between reproduction and immunity is likely able for reproduction. Second, mate choice can reduce disease affected by the mating system and the degree of twofold, both to the actor, by choosing healthy noninfectious sexual conflict. Reproduction and immunity seem mates, and by reducing risk to the offspring by acquiring protec- connected in three ways by resource trade-offs tive genes for the next generation (reviewed in Lawniczak et al., among life-history traits, by disease reduction due 2007). Finally, mating can directly affect immune responses, to mate choice of healthy mates and protective which then determines disease susceptibility. The nature of this genes for the offspring and by mating-induced relationship is likely tightly connected to the mating system (see immunity to reduce infection risk. also: Polyandry and Mating System Evolution) and hence the degree of Sexual Conflict. Here, we focus on the latter connection between mating and immunity as the others have been reviewed thoroughly elsewhere (Lawniczak et al., 2007; Siva-Jothy, 2009; Introduction Morrow and Innocenti, 2012; Schwenke et al., 2016). There is a striking parallel between immunity and reproduction The origin and maintenance of sexual reproduction have endured at their shared fundament: the detection of ‘other’. During infec- as a central question in evolutionary biology. Sexual reproduc- tion, this is obvious, if not simple. The task of a host is to identify tion can involve complicated behaviours and physiological pro- the nonself and destroy it to prevent harm. The reality is far more cesses that reflect both evolution to optimise sexual reproduction complicated, as it can result in failures to detect pathogens, result- overall but also as a consequence of an evolutionary arms race ing in greater pathology, or failure to ignore self, resulting in autoimmune responses. In sexual reproduction, processes of iden- eLS subject area: Evolution & Diversity of Life tification are no less important. Individuals, as well as gametes, How to cite: must be able to identify appropriate partners while also, prefer- Barribeau, Seth M and Otti, Oliver (July 2020) Sexual ably, not reproducing with kin to avoid potential costs of inbreed- Reproduction and Immunity. In: eLS. John Wiley & Sons, Ltd: ing (Lihoreau et al., 2008; Ylönen and Haapakoski, 2016). When Chichester. looking at the origin of the link between reproduction and immu- DOI: 10.1002/9780470015902.a0028146 nity, this connection becomes apparent (Box 1). The first sexually eLS © 2020, John Wiley & Sons, Ltd. www.els.net 1 k k Sexual Reproduction and Immunity Box 1 Ancient link between reproduction and immunity The molecular choice mechanisms in Sexual Selection may have been the evolutionary precursor of the recognition system in the vertebrate immune system (Boehm, 2006b). This, perhaps surprising, hypothesis is based on some similarities in how unicellular eukaryotes, such as fungi, and plants determine whether to sexually reproduce with another individual based on self/nonself (SNS) recognition (see also: Innate Immune Mechanisms: Nonself Recognition), which avoids inbreeding and an analogous process by which multicellular organisms use SNS discrimination in immune defence (Boehm, 2006a,2006b; Sanabria et al., 2008); hinting at a very early link of sexual reproduction and immunity. While an intriguing, and in some ways appealing hypothesis, data are limited to support the proposition. In plants, a similar speculation has been suggested about the clear parallels between self-incompatibility alleles and disease recognition alleles (Sanabria et al., 2008) (Box 2). In sexually reproducing animals, the mechanisms which result in the differential success or differential utilisation of sperm depend on the recognition of gametes are in many cases likely to be immunological as well (Birkhead and Møller, 1998). Vertebrates also appear to use immunological mechanisms in mate choice. The Major Histocompatibility Complex (MHC) is primarily used in the presentation of antigens in the immune response, but in a number of studies across vertebrates, it has been implicated in mate choice (Milinski et al., 2005; Milinski, 2006; Ziegler et al., 2005). Because the major histocompatibility complex (MHC) is highly polymorphic, it serves as a reliable signal of genetic similarity to oneself, and odours produced by ligands can be detected by the opposite sex (Milinski et al., 2005; Milinski, 2006; Ziegler et al., 2005). In mammals, the complex chemical signals are sensed by the vomeronasal organ and provide conspecifics with information on an individual’s sex, social and reproductive status (He et al., 2008). Vertebrate females might even perform cryptic female choice (see also: Post-copulatory Reproductive Strategies) and select sperm or ejaculates with a favourable MHC haplotype for the fertilisation of their eggs to optimise MHC alleles in their offspring (Firman et al., 2017; Milinski, 2006). In red junglefowl, females favour sperm from males that are dissimilar in their MHC (Løvlie et al., 2013) and female sticklebacks bias fertilisation towards optimal combinations of MHC haplotypes that maximise offspring fitness (Lenz et al., 2018). Self-incompatibility and more generally genetic incompatibility between mating partners caused by nonoptimal combinations of alleles from the MHC (Kalbe et al., 2009) or other immune genes as shown in humans (Hart et al., 2018) and plants (Chae et al., 2014) might align selection pressure on reproduction and immunity, therefore, maintaining the link. We hypothesise k that the ancient link between reproduction and immunity has set the scene or was the precursor of the derived links between k reproduction and immunity, such as self-incompatibility induced via immune gene incompatibilities in plants (Chae et al., 2014) and mate choice based on the MHC alleles (Firman et al., 2017; Milinski, 2006; Kalbe et al., 2009). Box 2 The case for plants Fertilisation and immunity in plants. Similar selection pressures seem to have shaped the link between fertilisation and immunity in plants. Especially, in flowering plants, the apparent similarity between self-incompatibility alleles and disease recognition alleles was identified a decade ago (Sanabria et al., 2008) although it is not clear whether this parallel is an example of homologous or analogous adaptations. Even though this is perhaps not directly relevant to the induction of post-fertilisation immunity; nectar and nectaries appear to contain many disease resistance-associated proteins (Zhou et al., 2016; Sasu et al., 2010). Another important selection pressure that has potentially led to a link between fertilisation and immunity in plants is the large body of evidence on pollinator transmitted diseases (Antonovics, 2005). While the process of fertilisation does induce the expression of immune genes (e.g. Mondragón-Palomino et al., 2017; Zhang et al., 2017), we do not know of any study that has examined post-fertilisation induction of immunity, for example upregulation of antimicrobials in nectar, in nectaries or in vegetative tissues and the role of this immune response on functional defences
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